Abstract
The retinal pigment epithelium (RPE) interacts with the photoreceptors, which it faces across the subretinal space. In these interactions the RPE acts as three types of cell - epithelium, macrophage, and glia. This review briefly describes selected interactions between the RPE and photoreceptors in ion and water transport, Vitamin A transport, phagocytosis of shed portions of outer segments, ensheathment of photoreceptors outer segments, and electrical responses. The electrical interactions can be recorded at the cornea in the c-wave, fast oscillation, and light peak of the DC electroretinogram (DC-ERG) and electrooculogram (EOG). Each response reflects photoreceptor-RPE interactions in a distinct way. The three responses taken together provide perhaps the best opportunity to learn how pathophysiological conditions alter the interactions between the RPE and photoreceptors.
This is a preview of subscription content, access via your institution.
References
Anderson DH, Stern WH, Fisher SK, Erikson PA and Borgula GA (1983) Retinal detachment in the cat: the pigment epithelial-photoreceptor interface. Invest Ophthalmol Vis Sci 24:906–926
Besharse JC (1980) Light and membrane biogenesis in rod photoreceptors of vertebrates. In: The effects of constant light on visual processes, Eds: Williams TP & Baker BN, New York, Plenum Publishing Co. pp 409–431
Bok D (1982) Autoradiograpic studies on the polarity of plasma membrane receptors in retinal pigment epithelial cells. In: The structure of the eye, Hollyfied J. Amsterdam, Elsevier, North Holland, pp 247–256
Bok D and Filerman B (1979) Localization of Na+, K+ ATPase in retinal photoreceptors and RPE with 3H-ouabain. Invest Ophthalmol Vis Sci 18 (Suppl): 224
Bok D and Heller J (1976) Transport of retinol from the blood to the retina: An autoradiographic study of the pigment epithelial cell surface receptor for plasma retinolbinding protein. Exp Eye Res 22:395–402
Bok D and Young R (1979) Phagocytic properties of the retinal pigment epithelium. In: The retinal pigment epithelium eds: Zinn KM and Marmor MF, Cambridge, Mass, Harvard University Press pp 148–174
Bridges CDB, Fong S-L, Liou GI, Alvarez RA and Landers RA (1983) Transport, utilization and metabolism of visual cycle retinoids in the retina and pigment epithelium. In: Progress in retinal research, Vol II, Eds: Osborne NW and Chader G Oxford, Pergamon Press Vol II, pp 137–162
Burnside MB (1976) Possible roles of microtubules and actin filaments in retinal pigmented epithelium. Exp Ey Res 23:257–275
Burnside B and Laties AM (1979) Pigment movement and cellular contractility in the retinal pigment epithelium. In: The retinal pigment epithelium, Marmor MF and Zinn KM, Cambridge, Mass, Harvard University Press, pp 175–191
Chader G (1982) Retinoids in ocular tissue: binding proteins, transport and mechanism of action. In: Cell biology of the eye, Ed: McDevitt D, New York, Academic Press, pp 377–433
Chader GJ, Wiggert B, Lai Y-L, Lee L and Fletcher RT (1983) Interphotoreceptor retinol-binding protein: a possible role in retinol transport to the retina. In: Progress in retinal research, Vol II, Eds: Osborne NN and Chader G, Oxford, Pergamon Press, pp 164–184
Faber DS (1969) Analysis of the slow transretinal potentials in response to light (Ph.D. Thesis) Buffalo, State University of New York
Feeney L (1978) Lipofuscin and melanin of human retinal pigment epithelium. Invest Ophthalmol Vis Sci 17:583–600
Feeney-Burns L, Hildebrand ES and Eldridge S (1984) Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells. Invest Ophthalmol Vis Sci 25:195–200
Fisher SK and Steinberg RH (1982) Origin and organization of pigment epithelial apical projections to cones in cat retina. J Comp Neurol 206:131–145
Fisher SK, Pfeffer DA and Anderson DH (1983) Both rod and cone disc shedding are related to light onset in the cat. Invest. Ophthalmol Vis Sci 24: 844–856
Frambach DA and Marmor MF (1982) The rate and route of fluid resorption from the subretinal space of the rabbit. Invest Ophthalmol Vis Sci 22:292–302
Griff ER and Steinberg RH (1982) Origin of the light peak: in vitro study of Gekko gekko. J Physiol (London) 331:637–652
Griff ER and Steinberg RH (1984) Changes in apical [K+]0 produce delayed basal membrane responses of the retinal pigment epithelium in the gecko. J Gen Physiol 83:193–211
Griff ER, Shirao Y and Steinberg RH (1984) Light-evoked slowing of RPE Na+-K+ pump unmasked b barium. Invest Ophthalmol Vis Sci (Suppl) 25:289
Hebel R (1970) Elektronenmikroskopische Untersuchung über den Bau und die Funktion des Pigmentepithels des Hundes. Z Anat Entwicklungs Gesh 130:115–128
Heller J (1975) Interactions of plasma retinol-binding protein with its receptor: Specific binding of bovine and human retinol-binding protein to pigment epithelium cells from bovine eyes. J Biol Chem 250:3613–3619
Herman KG and Steinberg RH (1982) Phagosome degradation in the tapetal retinal pigment epithelium of the opossum. Invest Ophthalmol Vis Sci 23:291–304
Hughes BA, Miller SS and Machen TE (1984) Effects of cAMP on fluid absorption and ion transport across frog retinal pigment epithelium: Measurement in the opencircuit state. J Gen Physiol 83: 875–899
Karwoski CJ and Proenza LM (1977) Relationship between Müller cell responses, a local transretinal potential, and potassium flux. J Neurophysiol 40:244–259
Karwoski CJ and Proenza LM (1981) Spatio-temporal variables in the relationship of neuronal activity to potassium and glial responses. Vision Res 21:1713–1718
Kolder H and Brecher GA (1966) Fast oscillations of the corneo-retinal potential in man. Arch Ophthalmol 75:232–237
Kolder H and North AW (1966) Oscillations of the corneo-retinal potential in animals. Ophthalmologica, Basel 152:149–160
Kuffler SW and Nicholls JG (1966) The physiology of neuroglial cells. Ergebn Physiol 57:1–90
Lasansky A and DeFisch FW (1966) Potential, current and ionic fluxes across the isolated retinal pigment epithelium and choroid. J Gen Physiol 49:913–924
La Vail M (1976) Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science 194:1071–1074
La Vail M (1980) Circadian nature of rod outer segment disc shedding in the rat. Invest Ophthalmol Vis Sci 19:407–411
Linsenmeier RA and Steinberg RH (1982) Origin and sensitivity of the light peak of the intact cat eye. J Physiol (London) 331:653–673
Linsenmeier RA and Steinberg RH (1984) Delayed basal hyperpolarization of cat retinal pigment epithelium, and its relation to the fast oscillation of the DC ERG. J Gen Physiol 83:213–232
Linsenmeier RA and Steinberg RH (1985a) Effects of hypoxia on potassium homeostasis and pigment epithelial cells in the cat retina. J Gen Physiol 84:945–970
Linsenmeier RA and Steinberg RH (1985b) Mechanisms of hypoxic effects on the cat DC electroretinogram. Invest Ophthalmol Vis Sci (in press)
Linsenmeier RA, Mines AH and Steinberg RH (1985) Effects of hypoxia and hypercapnia on the light peak and electroretinogram of the cat. Invest Ophthalmol Vis Sci 24:37–46
Maraini G (1979) Binding for retinol in retina and pigment epithelium. In: Current topics in eye research, Vol. I, Eds: Zadunaisky J and Davson H, New York, Academic press pp. 143–174
Maraini G and Gozzoli F (1975) Binding of retinol to isolated retinal pigment epithelium in the presence and absence of retinol-binding protein. Invest Ophthalmol 14:785–787
Marmor F and Maack T (1982a) Enhancement of retinal adhesion and subretinal fluid resorption by acetazolamide. Invest Ophthalmol Vis Sci 23:121–124
Marmor F and Maack T (1982b) Local environmental factors and retinal adhesion in the rabbit. Exp Eye Res 34:727–733
Matsuura T, Miller WH and Tomita T (1978) Cone-specific c-wave in the turtle retina. Vision Res 18:767–775
Miller S and Farber D (1984) Cyclic AMP modulation of ion transport across frog retinal pigment epithelium: measurements in the short-circuit state. J Gen Physiol 83:853–874
Miller SS and Steinberg RH (1977a) Passive ionic properties of frog retinal pigment epithelium. J Membr Biol 36:337–372
Miller SS and Steinberg RH (1977b) Active transport of ions across frog retinal pigment epithelium. Exp Eye Res 25:235–248
Miller SS and Steinberg RH (1982) Potassium transport across the frog retinal pigment epithelium. J Membrane Biol 67:199–209
Miller SS, Steinberg RH and Oakley B II (1978) The electrogenic sodium pump of the frog retinal pigment epithelium. J Membr Biol 44:259–279
Miller SS, Hughes B and Machen TE (1982) Fluid transport across the retinal pigment epithelium is inhibited by cyclic AMP. Proc Natl Acad Sci USA 79:2111–2115
Negi A and Marmor M (1983) The resorption of subretinal fluid after diffuse damage to the retinal pigment epithelium. Invest Ophthalmol Vis Sci 24:1475–1479
Negi A and Marmor M (1984) Experimental serous retinal detachment and focal pigment epithelial damage. Arch Ophthalmol 102:445–449
Niemeyer G, Nagahara K and Demant E (1982) Effects of changes in arterial PO2 and PCO2 on the ERG in the cat. Invest Ophthalmol Vis Sci 23:678–683
Niemeyer G and Steinberg RH (1984) Differential effects of PCO[in2] and pH on the ERG and light peak of the perfused cat eye. Vision Res 24:275–280
Oakley B II, Flaming DG and Brown KT (1979) Effects of the rod receptor potential upon extracellular potassium ion concentration. J Gen Physiol 74:713–737
Oakley B II and Green DG (1976) Correlation of light-induced changes in retinal extracellular potassium concentration with the c-wave of the electroretinogram. J Neurophysiol 39:1117–1133
Oakley B II, Miller SS and Steinberg RH (1978) Effects of intracellular potassium upon the electrogenic pump of frog retinal pigment epithelium. J Membrane Biol 44:281–307
Ostwald TJ and Steinberg RH (1979) Retinal pigment epithelium Na-K ATPase: Characterization and apical membrane localization in the frog. Invest Ophthalmol Vis Sci (Suppl): 268
Ostwald TJ and Steinberg RH (1980) Localization of frog retinal pigment epithelium Na+-Ka+ ATPase. Ex Res 31:351–360
Rodieck RW (1972) Components of the electroretinogram - a reappraisal. Vision Res 12:773–780
Rodieck RW (1973) The vertebrate retina, San Francisco, W H Freeman
Rosenbluth J (1962) The fine structure of acoustic ganglia in the rat. J Cell Biol 12: 329–359
Rosenbluth J and Palay S (1961) The fine structure of nerve cell bodies and their myelin sheaths in the eight nerve ganglion of the goldfish. J Biophys Biochem Cytol 9: 853–877
Saari J and Futterman S (1976) Separable binding proteins for retinoic acid and retinol in bovine retina. Biochim Biophys Acta 444:789–793
Saari J, Futterman S and Bredberg L (1978) Cellular retinol- and retinoic acid-binding proteins of bovine retina: Purification and properties. J Biol Chem 253:6432–6436
Scullica L and Tangucci F (1968) The ultrastructural relationship between pigment cells and photoreceptors. J Microscopie 7:1085–1092
Shimazaki H and Oakley B II (1984) Reaccumulation of [K+]0 in a toad retina during maintained illumination. J Gen Physiol 84:475–504
Sjöstrand FS and Nilsson SE (1964) The structure of the rabbit retina as revealed by electronmicroscopy. In: The rabbit in eye research, Ed: Prince JH, Springfield, Charles C Thomas, pp 1–65
Steinberg RH and Miller SS (1973) Aspects of electrolyte transport in frog epithelium. Exp Eye Res 16:365–372
Steinberg RH and Miller SS (1979) Transport and membrane properties of the retinal pigment epithelium. In: The retinal pigment epithelium, Eds: Zinn KM and Marmor MF, Cambridge, Mass, Harvard University, pp 205–225
Steinberg RH and Niemeyer G (1981) Eight peak of cat DC electroretinogram: not generated by a change in [K+]0]. Invest Ophthalmol Vis Sci 20:414–418
Steinberg RH and Wood I (1974) Pigment epithelial cell ensheathment of cone outer segments in the retina of the domestic cat. Proc R Soc Lond [Biol] 187:461–478
Steinberg RH, Schmidt R and Brown KT (1970) Intracellular responses to light from the cat retinal pigment epithelium: origin of the electroretinogram c-wave. Nature 227:728–730
Steinberg RH, Wood I and Hogan MJ (1977) Pigment epithelial ensheathment and phagocytosis of extrafoveal cones in human retina. Philos. Trans R Soc Eond [Biol] 277:459–474
Steinberg RH, Linsenmeier RA and Griff ER (1985) Retinal pigment epithelial cell contributions to the electroretinogram and electrooculogram In: Progress in retinal research, Vol. IV Eds: Osborne N and Chader I. Oxford, Pergamon Press, pp. 33–66
Valeton JM and van Norren D (1982) Intraretinal recordings of slow electrical responses to steady illumination in monkey: isolation of receptor responses and the origin of the light peak. Vision Res 22:393–399
Wiggert B and Chader G (1975) A receptor for retinol in the developing retina and pigment epithelium. Exp Eye Res 21:143–151
Young RW (1967) The renewal of photoreceptor cell outer segments. J Cell Biol 33: 61–72
Young RW and Bok D (1969) Participation of the retinal pigment epithelium in the rod outer segment renewal process. J Cell Biol 42:392–403
Zadunaisky JA and Degnan KJ (1976) Passage of sugars and urea across the isolated retina pigment epithelium of the frog. Exp Eye Res 23:191–196
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Steinberg, R.H. Interactions between the retinal pigment epithelium and the neural retina. Doc Ophthalmol 60, 327–346 (1985). https://doi.org/10.1007/BF00158922
Issue Date:
DOI: https://doi.org/10.1007/BF00158922
Key words
- electrooculogram
- electroretinogram
- photoreceptor
- retinal pigment epithelium