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Lamellar to tubular conformational changes in the endoplasmic reticulum of the retinal pigment epithelium of the newt, Notophthalmus viridescens

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Summary

The retinal pigment epithelium (RPE) of the newt (Notophthalmus viridescens) was examined ultrastructurally under both in-vivo and in-vitro conditions. Five distinct conformations of smooth endoplasmic reticulum (SER), two lamellar and three tubular, were observed. The two lamellar conformations included myeloid bodies, which have previously been described (Yorke and Dickson 1984), and fenestrated SER. The latter appeared as layers of flattened or curved cisternae which were penetrated by fenestrations. Fenestrated SER became indistinguishable from the highly branched and convoluted random-tubular SER through the formation of an intermediate configuration (“tubular sheets”). The remaining tubular SER conformations appeared to arise from random-tubular SER through a progressive reduction in branching and a straightening of individual tubules. Fascicular SER was represented by the hexagonal organization of straight, unbranched tubules into bundles (fascicles). Spiral SER consisted of a similar hexagonal arrangement, but the unbranched tubules spiralled about one another. Neighbouring tubules in areas of spiral SER were also joined together by pairs of electrondense bars. Although lamellar (especially myeloid bodies) and random-tubular configurations of the SER were common features in vivo, fascicular and spiral SER were primarily conformations encountered in vitro. Conditions favouring bilayer lipid phases also appear to facilitate the formation of both myeloid bodies and fascicular SER. These conditions included increased duration of incubation, low (<20° C) incubation temperatures, and Ca2+-free incubations with EGTA. Random-tubular SER was most prevalent in media supplemented with fetal calf serum and also after warmer (30° C) incubation temperatures. We speculate that the different conformations of SER observed in the newt RPE may be due, in part, to lipid phase transitions within the membranes of this organelle. However, the specific formation of fascicular and spiral SER may also involve some additional factor, possibly a protein.

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References

  • Alonso G, Assenmacher I (1979) Three-dimensional organization of the endoplasmic reticulum in supraoptic neurons of the rat. A structural functional correlation. Brain Res 170:247–258

    Google Scholar 

  • Basu PK, Sarkar P, Menon I, Carré F, Persad S (1983) Bovine retinal pigment epithelial cells cultured in vitro: growth characteristics, morphology, chromosomes, phagocytosis ability, tyrosinase activity and the effect of freezing. Exp Eye Res 36:671–684

    Google Scholar 

  • Boggs JM (1980) Intermolecular hydrogen bonding between lipids: influence on organization and function of lipids in membranes. Can J Biochem 58:755–770

    Google Scholar 

  • Borovjagin VL, Vergara JA, McIntosh TJ (1982) Morphology of the intermediate stages in the lamellar to hexagonal lipid phase transition. J Membr Biol 69:199–212

    Google Scholar 

  • Buchheim W, Drenckhahn D, Lüllmann-Rauch R (1979) Freezefracture studies of cytoplasmic inclusions occurring in experimental lipidosis as induced by amphiphilic cationic drugs. Biochim Biophys Acta 575:71–80

    Google Scholar 

  • Büldt G, Wohlgemuth R (1981) The headgroup conformation of phospholipids in membranes. J Membr Biol 58:81–100

    Google Scholar 

  • Burger PC, Herson PB (1966) Phenobarbital-induced fine structural changes in rat liver. Am J Pathol 48:793–809

    Google Scholar 

  • Chin DJ, Luskey KL, Anderson RGW, Faust JR, Goldstein JL, Brown MS (1982) Appearance of crystalloid endoplasmic reticulum in compactin-resistant Chinese hamster cells with a 500-fold increase in 3-hydroxy-3-methylglutaryl-coenzyme-A reductase. Proc Natl Acad Sci 79:1185–1189

    Google Scholar 

  • Christensen AK (1965) The fine structure of testicular interstitial cells in guinea pigs. J Cell Biol 26:911–936

    Google Scholar 

  • Christensen AK, Fawcett DW (1966) The fine structure of testicular interstitial cells in mice. Am J Anat 118:551–572

    Google Scholar 

  • Cullis PR, Dr Kruijff B (1979) Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta 559:399–420

    Google Scholar 

  • Cullis PR, Verkleij AJ (1979) Modulation of membrane structure by Ca2+ and dibucaine as detected by 31P NMR. Biochim Biophys Acta 552:546–551

    Google Scholar 

  • Cullis PR, Dr Kruijff B, Hope MJ, Nayer R, Schmidt SL (1980) Phospholipids and membrane transport. Can J Biochem 58:1091–1100

    Google Scholar 

  • Davis DG, Inesi G (1971) Proton nuclear magnetic resonance studies of sarcoplasmic reticulum membranes. Correlation of the temperature-dependent Ca2+ efflux with a reversible structural transition. Biochim Biophys Acta 241:1–8

    Google Scholar 

  • Deese AJ, Dratz EA, Brown MF (1981) Retinal rod outer segment lipids form bilayers in the presence and absence of rhodopsin: a 31P NMR study. FEBS Lett 124:93–99

    Google Scholar 

  • De Kruijff B, Van Den Besselaar AMHP, Cullis PR, Van Den Bosch H, Van Deenen LLM (1978) Evidence for isotropic motion of phospholipids in liver microsomal membranes. Biochim Biophys Acta 514:1–8

    PubMed  Google Scholar 

  • Dickson DH, Hollenberg MJ (1971) The fine structure of the pigment epithelium and photoreceptor cells of the newt, Triturus viridescens dorsalis (Rafinesque). J Morphol 135:389–432

    Google Scholar 

  • Flood MT, Gouras P, Kjeldbye H (1980) Growth characteristics and ultrastructure of human retinal pigment erpithelium in vitro. Invest Ophthalmol Vis Sci 19:1309–1320

    Google Scholar 

  • Greenberger LM, Besharse JC (1983) Photoreceptor disc shedding in eye cups. Inhibition by deletion of extracellular divalent cations. Invest Ophthalmol Vis Sci 24:1456–1464

    Google Scholar 

  • Israel P, Masterson E, Goldman AI, Wiggert B, Chader GJ (1980) Retinal pigment epithelial cell differentiation in vitro. Influence of culture medium. Invest Ophthalmol Vis Sci 19:720–727

    Google Scholar 

  • Kuwabara T (1975) Cytologic changes of the retina and pigment epithelium during hibernation. Invest Ophthalmol 14:457–467

    Google Scholar 

  • Marshall J, Ansell PJ (1971) Membranous inclusions in the retinal pigment epithelium: phagosomes and myeloid bodies. J Anat 110:91–104

    Google Scholar 

  • Nayar R, Schmid SL, Hope MJ, Cullis PR (1982) Structural preferences of phosphatidylinositol and phosphatidylinositol-phosphatidylethanolamine model membranes. Influence of Ca2+ and Mg2+. Biochim Biophys Acta 668:169–176

    Google Scholar 

  • Nguyen-Legros J (1975) A propos des corps myéloïdes de l'épithélium pigmentaire de la rétine des vertébrés. J Ultrastruc Res 53:152–163

    Google Scholar 

  • Nguyen-Legros J (1978) Fine structure of the pigment epithelium in the vertebrate retina. Inter Rev Cytol (Suppl) 7:287–328

    Google Scholar 

  • Nguyen-Legros J, Marchi N (1974) Les corps myéloïdes de l'épithélium pigmentaire rétinien. III. Compartiment en culture de tissus. Micron 5:21–39

    Google Scholar 

  • Novikoff AB, Spater HW, Quintana N (1983) Transepithelial endoplasmic reticulum in rat proximal convoluted tubule. J Histochem Cytochem 31:656–661

    Google Scholar 

  • O'Leary TJ (1983) A simple theoretical model for the effects of cholesterol and polypeptides on lipid membranes. Biochim Biophys Acta 731:47–53

    Google Scholar 

  • Porter KR, Yamada E (1960) Studies on the endoplasmic reticulum V. Its form and differentiation in pigment epithelial cells of the frog retina. J Biophys Biochem Cytol 8:181–205

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–213

    Article  CAS  PubMed  Google Scholar 

  • Stier A, Finch SAE, Bösterling B (1978) Non-lamellar structure in rabbit liver microsomal membranes. An 31P-NMR study. FEBS Lett 91:109–112

    Google Scholar 

  • Stramm LE, Haskins ME, McGovern MM, Aguirre GD (1983) Tissue culture of cat retinal pigment epithelium. Exp Eye Res 36:91–102

    Google Scholar 

  • Thorsch J, Esau K (1981) Changes in the endoplasmic reticulum during differentiation of a sieve element in Gossypium hirsutum. J Ultrastruct Res 74:183–194

    Google Scholar 

  • Thys O, Hildebrand J, Gérin Y, Jacques PJ (1973) Alterations of rat liver lyososomes and smooth endoplasmic reticulum induced by the diazafluoranthen derivative AC-3579. I. Morphologic and biochemical lesions. Lab Invest 28:70–82

    Google Scholar 

  • Yorke MA, Dickson DH (1984) Diurnal variations in myeloid bodies of the newt retinal pigment epithelium. Cell Tissue Res 235:177–186

    Google Scholar 

  • Yorke MA, Dickson DH (1985) Evidence for retinyl esters associated with myeloid bodies in the newt retinal pigment epithelium. Cell Tissue Res 240:641–648

    Google Scholar 

  • Zinn KM, Benjamin-Henkind JV (1979) Anatomy of the human retinal pigment epithelium. In: Zinn KM, Marmor MF (eds) The retinal pigment epithelium. Harvard Univ Press, Cambridge, Mass

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Dalhousie University, Halifax, Canada

    Marc A. Yorke &  D. Howard Dickson

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  1. Marc A. Yorke
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  2. D. Howard Dickson
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Supported by grant # MT-5039 from the Medical Research Council of Canada to DHD

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Yorke, M.A., Dickson, D.H. Lamellar to tubular conformational changes in the endoplasmic reticulum of the retinal pigment epithelium of the newt, Notophthalmus viridescens . Cell Tissue Res. 241, 629–637 (1985). https://doi.org/10.1007/BF00214585

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