Abstract
Immunohistochemical and physiological studies on various insect photoreceptors have demonstrated that the Na,K-ATPase (sodium pump) is restricted to the nonreceptive nonmicrovillar area of the plasma membrane. Here, we examined the distribution of the Na,K-ATPase in photoreceptor cells of the superposition-type compound eye in the moth Manduca sexta. Using immunofluorescent and immunogold cytochemistry, we show that the Na,K-ATPase is localized to both the nonmicrovillar and the microvillar parts of the plasma membrane. Manduca photoreceptors thus deviate from the common concept that the sodium pump and the molecular components of the photoreceptive machinery reside on different domains of the plasma membrane.
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Arikawa K, Hicks JL, Williams DS (1990) Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110:1993–1998
Bacigalupo J, Lisman JE (1983) Single-channel currents activated by light in Limulus ventral nerve photoreceptors. Nature 304:268–270
Baumann O (1992) Structural interactions of actin filaments and endoplasmic reticulum in honeybee photoreceptor cells. Cell Tissue Res 268:71–79
Baumann O, Takeyasu K (1993) Polarized distribution of Na,K-ATPase in honeybee photoreceptors is maintained by interaction with glial cells. J Cell Sci 105:287–301
Baumann O, Walz B, Somlyo AV, Somlyo AP (1991) Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors. Proc Natl Acad Sci USA 88:741–744
Baumann O, Lautenschläger B, Takeyasu K (1994) Immunolocalization of Na,K-ATPase in blowfly photoreceptor cells. Cell Tissue Res 275:225–234
Bell RA, Joachim FA (1976) Techniques for rearing laboratory colonies of tabacco hornworms and pink bollworms. Ann Ent Soc Am 69:365–373
Boschek CB, Hamdorf K (1976) Rhodopsin particles in the photoreceptor membrane of an insect. Z Naturforsch 31 C:762–763
Byers TJ, Dubreuil R, Branton D, Kiehart DP, Goldstein LSB (1987) Drosophila spectrin. II. Conserved features of the alpha subunit are revealed by analysis of cDNA clones and fusion proteins. J Cell Biol 105:2103–2110
Chi C, Carlson SD (1981) Lanthanum and freeze fracture studies on the retinula cell junction in the compound eye of the house-fly. Cell Tisse Res 214:541–552
Coles JA, Orkand RK (1985) Changes in sodium activity during light stimulation in photoreceptors, glia and extracellular space in drone retina. J Physiol (Lond) 362:415–435
Coles JA, Orkand RK, Yamate CL, Tsacopoulos M (1987) Free concentrations of Na, K, and Cl in the retina of the honeybee drone: stimulus-induced redistribution and homeostasis. Ann N Y Acad Sci 481:303–317
Danscher G (1981) Localization of gold in biological tissue. Histochemistry 71:81–88
Dimitracos SA, Tsacopoulos M (1985) The recovery from a transient inhibition of the oxidative metabolism of the photoreceptors of the drone (Apis mellifera ♂). J Exp Biol 119:165–181
Faulstich HS, Zobeley S, Rinnerthaler G, Small JV (1988) Fluorescent phallotoxins as probes for filamentous actin. J Muscle Res Cell Motil 1:89–100
Fulpius B, Baumann F (1969) Effects of sodium, potassium and calcium ions on slow and spike potentials in single photoreceptor cells. J Gen Physiol 53:541–561
Goldsmith TH, Wehner R (1977) Restriction on the rotational and translational diffusion of pigment in the membranes of a rhabdomeric photorector. J Gen Physiol 70:453–490
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 [Biol] 245:203–210
Horisherger J-D, Lemas V, Krähenbühl, J-P, Rossier BC (1991) Structure-function relationship of Na,K-ATPase. Annu Rev Physiol 53:565–584
Horowitz B, Eakle KA, Scheiner-Bobis G, Randolph GR, Chen CY, Hitzeman RA, Farley RA (1990) Synthesis and assembly of functional mammalian Na,K-ATPase in yeast. J Biol Chem 265:4189–4192
Jaisser F, Canessa CM, Horisberger J-D, Rossier BC (1992) Primary sequence and functional expression of a novel ouabain-resistant Na,K-ATPase — the beta subunit modulates potassium activation of the Na,K-pump. J Biol Chem 267:16895–16903
Jansonius NM (1990) Properties of sodium pump in the blowfly photoreceptor cell. J Comp Physiol [A] 167:461–467
Jaunin P, Jaisser F, Beggah AT, Takeyasu K, Mangeat P, Rossier BC, Horisberger J-D, Geering K (1993) Role of transmembrane and extracytoplasmic domain of β subunits in subunit assembly, intracellular transport, and functional expression of Na,K-pumps. J Cell Biol 123:1751–1759
Klein U, Zimmermann B (1991) The vacuolar-type ATPase from insect plasma membrane: immunocytochemical localization in insect sensilla. Cell Tissue Res 266:265–273
Kone BC, Takeyasu K, Fambrough DM (1991) Structure-function studies on the Na,K-ATPase isozymes. In: Kaplan JH, De Weer P (eds) The sodium pump: recent developments, vol 46. Society of the General Physiologists Series, Rockefeller University Press, New York, pp 265–269
Kushmerick MJ, Podolsky RJ (1969) Ionic mobility in muscle cells. Science 166:1297–1298
Langer M, Thorell B (1966) Microspectrophotometry of single rhabdomeres in an insect eye. Exp Cell Res 41:673–677
Langer M, Schmeinck G, Anton-Erxleben F (1986) Identification and localization of visual pigments in the retina of the moth, Antheraea polyphemus (Insecta, Saturniidae). Cell Tissue Res 245:81–86
Lebovitz RM, Takeyasu K, Fambrough DM (1989) Molecular characterization and expression of the (Na++K+)-ATPase alpha-subunit in Drosophila melanogaster. EMBO J 8:193–202
Madreperla SA, Edidin M, Adler R (1989) Na+, K+-adenosine trisphosphatase polarity in retinal photoreceptors: a role for cytoskeletal attachments. J Cell Biol 109:1483–1493
Meinecke CC (1981) The fine structure of the compound eye of the African armyworm moth, Spodoptera exempta walk. (Lepidoptera, Noctuidae). Cell Tissue Res 216:333–347
McDonough AA, Geering K, Farley RA (1990) The sodium pump needs its β subunit. FASEB J 4:1598–1605
Nilsson D-E (1989) Optics and evolution of the compound eye. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 30–73
Payne R, Fein A (1984) Localization of the photocurrent of Limulus ventral photoreceptors using a vibrating probe. Biophys J 50:193–196
Perrelet A, Baumann F (1969) Evidence for extracellular space in the rhabdome of the honeybee eye. J Cell Biol 40:825–830
Ranganathan R, Harris GL, Stevens CF, Zuker CS (1991) A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization. Nature 354:230–232
Schneuwly S, Burg MG, Lending C, Perdew MH, Pak WL (1991) Properties of photoreceptor-specific phospholipase-C encoded by the norpA gene of Drosophila melanogaster. J Biol Chem 266:24314–24319
Shaw SR (1978) The extracellular space and blood-eye barrier in an insect retina: an ultrastructural study. Cell Tissue Res 188:35–61
Takeyasu K, Tamkun MM, Renaud KJ, Fambrough DM (1988) Ouabain-sensitive (Na++K+)-ATPase activity expressed in mouse L cells by transfection with DNA encoding the α-subunit of an avian sodium pump. J Biol Chem 263:4347–4354
Walz B (1985) Light-induced changes of extra- and intracellular potassium concentrations in the photoreceptors of the leech, Hirudo medicinalis. J Comp Physiol [A] 157:199–210
White RH, Bennett RR (1992) Rhabdomeric membrane and smooth endoplasmic reticulum in photoreceptors of Manduca sexta — modulations associated with the diurnal light/dark cycle and effects of chromophore deprivation. Cell Tissue Res 270:57–64
Wollner DA, Nelson WJ (1992) Establishing and maintaining epithelial cell polarity. J Cell Sci 102:185–190
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Baumann, O., Lautenschläger, B. Immunolocalization of the Na,K-ATPase in photoreceptor cells of the moth Manduca sexta-evidence for Na,K-ATPase on both the nonmicrovillar and the microvillar domains of the plasma membrane. Cell Tissue Res 281, 119–126 (1995). https://doi.org/10.1007/BF00307965
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DOI: https://doi.org/10.1007/BF00307965