Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T04:28:39.059Z Has data issue: false hasContentIssue false
  • English
  • Français

Variability in mitochondria of zebrafish photoreceptor ellipsoids

Published online by Cambridge University Press:  17 January 2014

R. TARBOUSH ,
I. NOVALES FLAMARIQUE ,
G.B. CHAPMAN  and
V.P. CONNAUGHTON
R. TARBOUSH
Affiliation:
Department of Biology, American University, Washington DC Present address: Department of Neurotrauma, Navy Medical Research Center, Silver Spring, Maryland 20910
I. NOVALES FLAMARIQUE
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada
G.B. CHAPMAN
Affiliation:
Department of Biology, Georgetown University, Washington DC
V.P. CONNAUGHTON*
Affiliation:
Department of Biology, American University, Washington DC
Get access Rights & Permissions [Opens in a new window]

Abstract

Ultrastructural examination of photoreceptor inner segment ellipsoids in larval (4, 8, and 15 days postfertilization; dpf) and adult zebrafish identified morphologically different types of mitochondria. All photoreceptors had mitochondria of different sizes (large and small). At 4 dpf, rods had small, moderately stained electron-dense mitochondria (E-DM), and two cone types could be distinguished: (1) those with electron-lucent mitochondria (E-LM) and (2) those with mitochondria of moderate electron density. These distinctions were also apparent at later ages (8 and 15 dpf). Rods from adult fish had fewer mitochondria than their corresponding cones. The ellipsoids of some fully differentiated single and double cones contained large E-DM with few cristae; these were surrounded by small E-LM with typical internal morphology. The mitochondria within the ellipsoids of other single cones showed similar electron density. Microspectrophotometry of cone ellipsoids from adult fish indicated that the large E-DM had a small absorbance peak (∼0.03 OD units) and did not contain cytochrome-c, but crocetin, a carotenoid found in old world monkeys. Crocetin functions to prevent oxidative damage to photoreceptors, suggesting that the ellipsoid mitochondria in adult zebrafish cones protect against apoptosis and function metabolically, rather than as a light filter.

Keywords

DevelopmentRetinaInner segment
Type
Research Articles
Information
Visual Neuroscience , Volume 31 , Issue 1 , January 2014 , pp. 11 - 23
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alison, W., Barthel, L., Skebo, K., Takechi, M., Kawamura, S. & Raymond, P. (2010). Ontogeny of cone photoreceptor mosaics in zebrafish. The Journal of Comparative Neurology 518, 4182–4195.CrossRefGoogle Scholar
Bowmaker, J., Astell, S., Hunt, D. & Mollon, J. (1991). Photosensitive and photostable pigments in the retinae of old world monkeys. The Journal of Experimental Biology 156, 1–19.Google Scholar
Branchek, T. & Bremiller, R. (1984). The development of photoreceptors in the zebrafish, Brachydanio rerio. I. Structure. The Journal of Comparative Neurology 224, 107–115.Google Scholar
Bui, B., Kalloniatis, M. & Vingrys, A. (2003). The contribution of glycolytic and oxidative pathways it retinal photoreceptor function. Investigative Ophthalmology & Visual Science 44, 2708–2715.CrossRefGoogle ScholarPubMed
Cameron, D. (2002). Mapping absorbance spectra, cone fractions, and neuronal mechanisms to photopic spectral sensitivity in the zebrafish. Visual Neuroscience 19, 365–372.Google Scholar
Chapman, G., Tarboush, R., Eagles, D. & Connaughton, V. (2009). A light and transmission electron microscope study of the distribution and ultrastructural features of peripheral nerve processes in the extra-retinal layers of the zebrafish eye. Tissue Cell 41, 286–298.CrossRefGoogle ScholarPubMed
Collins, S., Collins, H. & Ali, M. (1996). Ultrastructure and organization of the retina and pigment epithelium in the cutlips minnow, Exoglossum maxillingua (Cyprinidae, Teleostei). Histology and Histopathology 11, 55–69.Google Scholar
Connaughton, V. & Nelson, R. (2010). Spectral responses in zebrafish horizontal cells include a tetraphasic response and a novel UV-dominated triphasic response. Journal of Neurophysiology 104, 2407–2422.Google Scholar
Fishelson, L., Ayalon, G., Zverdling, A. & Holzman, R. (2004). Comparative morphology of the eye (with particular attention to the retina) in various species of cardinal fish (Apogonidae, Teleostei). Anatomical Record A: Discoveries in Molecular, Cellular, and Evolutionary Biology 227, 249–261.Google Scholar
Gibbons, I. & Grimstone, A. (1960). On flagellar structure in certain flagellates. The Journal of Cell Biology 7, 697–716.CrossRefGoogle ScholarPubMed
Goldsmith, T., Collins, J. & Licht, S. (1984). The cone oil droplets in avian retinas. Vision Research 24, 1661–1671.Google Scholar
Grun, G. (1975). Structural basis of the functional development of the retina in the cichlid Tilapia leucosticta (Teleostei). Journal of Embryology and Experimental Morphology 33, 243–257.Google Scholar
Hárosi, F. (1987). Cynomolgous and rhesus monkey visual pigments. Application sof Fourier transform smoothing and statistical techniques to the determination of spectral parameters. The Journal of General Physiology 89, 717–743.Google Scholar
Hárosi, F. (1994). An analysis of two spectral properties of vertebrate visual pigments. Vision Research 34, 1359–1367.CrossRefGoogle ScholarPubMed
Hárosi, F. & Novales Flamarique, I. (2012). Functional significance of the taper of vertebrate cone photoreceptors. The Journal of General Physiology 139, 159–187.Google Scholar
Haug, M., Biehlmaier, O., Mueller, K. & Neuhauss, S. (2010). Visual acuity in larval zebrafish: Behavior and histology. Frontiers in Zoology 78, 1–7.Google Scholar
Hayat, M. (2000). Principles and Techniques of Electron Microscopy. Cambridge: Cambridge University Press.Google Scholar
Hoang, Q., Linsenmeier, R., Chung, C. & Curcio, C. (2002). Photoreceptor inner segments in monkey and human retina: Mitochondrial density, optics, and regional variation. Visual Neuroscience 19, 395–407.CrossRefGoogle ScholarPubMed
Hughes, A., Saszik, S., Bilotta, J., DeMarco, P. Jr. & Patterson, W. II. (1998). Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience 15, 1029–1037.Google Scholar
Ishikawa, T. & Yamada, E. (1969). Atypical mitochondria in the ellipsoid of the photoreceptor cells of vertebrate retinas. Investigative Ophthalmology & Visual Science 8, 302–316.Google ScholarPubMed
Kim, J., Lee, E., Chang, B., Oh, C., Mun, G., Chung, Y. & Shin, D. (2005). The presence of megamitochondria in the ellipsoid of photoreceptor inner segment of the zebrafish retina. Anatomia, Histologia, Embryologia 34, 339–342.Google Scholar
Kljavin, I. (1987). Early development of photoreceptors in the ventral retina of the zebrafish embryo. The Journal of Comparative Neurology 260, 461–471.Google Scholar
Knabe, W., Skatchkov, S. & Kuhn, H.-J. (1997). “Lens mitochondria” in the retinal cones of the tree-shrew, Tupaia belangeri. Vision Research 37, 267–271.Google Scholar
Kunz, Y. (2006). Review of development and aging in the eye of teleost fish. Neuroembryol Aging 4, 31–60.Google Scholar
Larison, K. & Bremiller, R. (1990). Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development 109, 567–576.Google Scholar
Linton, J., Holzhausen, L., Babai, N., Song, H., Miyagishima, K., Stearns, G., Lindsay, K., Wei, J., Chertov, A., Peters, T., Caffe, R., Pluk, H., Seeliger, M., Tanimoto, N., Fong, K., Bolton, L., Kuok, D., Sweet, I., Bartoletti, T., Radu, R., Travis, G., Zagotta, W., Townes-Anderson, E., Parker, E., Van der Zee, C., Sampath, A., Sokolov, M., Thoreson, W. & Hurley, J. (2010). Flow of energy in the outer retina in darkness and in light. Proceedings of the National Academy of Sciences of the United States of America 107, 8599–8604.CrossRefGoogle ScholarPubMed
Lluch, S., Lopez-Fuster, M. & Ventura, J. (2003). Giant mitochondria in the retina cone inner segments of shrews of genus Sorex (Insectivora, Soricidae). Anatomical Record A: Discoveries in Molecular, Cellular, and Evolutionary Biology 272, 484–490.CrossRefGoogle ScholarPubMed
Luft, J.H. (1961). Improvements in epoxy resin embedding methods. J. Biophys. Biochem Cytol. 9, 409–414.CrossRefGoogle ScholarPubMed
MacNichol, E., Kunz, Y., Levine, J., Harosi, F. & Collins, B. (1978). Ellipsosomes: Organelles containing a cytochrome-like pigment in the retinal cones of certain fishes. Science 200, 549–552.Google Scholar
Mariani, A.P. (1987). Neuronal and synaptic organization of the outer plexiform layer of the pigeon retina. Am. J. Anat. 179, 25–39.CrossRefGoogle ScholarPubMed
McDowell, A., Dixon, L., Houchins, J. & Bilotta, J. (2004). Visual processing of the zebrafish optic tectum before and after optic nerve damage. Visual Neuroscience 21, 97–106.CrossRefGoogle ScholarPubMed
Millonig, G. (1961). Advantages of a phosphate buffer for osmium tetroxide solutions in fixation. Journal of Applied Physics 32, 1637–1639.Google Scholar
Nag, T. & Bhattacharjee, J. (1995). Retinal ellipsosomes: Morphology, development, identification, and comparison with oil droplets. Cell Tissue Research 279, 633–637.CrossRefGoogle ScholarPubMed
Nelson, R. & Singla, N. (2009). A spectral model for signal elements isolated from zebrafish photopic electroretinogram. Visual Neuroscience 26, 349–363.Google Scholar
Novales Flamarique, I. & Hárosi, F. (1999). Photoreceptor pigments of the blueback herring (Alosa aestevalis, Clupeidae) and the Atlantic silverside (Menidia menidia, Atherinidae). The Biological Bulletin 197, 235–236.Google Scholar
Novales Flamarique, I. & Hárosi, F. (2000). Photoreceptors, visual pigments, and ellipsosomes in the killifish, Fundulus heteroclitus: A microspectrophotometric and histological study. Visual Neuroscience 17, 403–420.Google Scholar
Novales Flamarique, I. & Hárosi, F. (2002). Visual pigments and dichroism of anchovy cones: A model system for polarization detection. Visual Neuroscience 19, 467–473.Google Scholar
Osinchak, J. (1964). Electron microscopic localization of acid phosphatase and thymine prophosphatase activity in hypothalamic neurosecretory cells of the rat. The Journal of Cell Biology 21, 3–48.Google Scholar
Pedler, C. & Boyle, M. (1969). Multiple oil droplets in the photoreceptors of the pigeon. Vision Research 9, 525–528.CrossRefGoogle ScholarPubMed
Perkins, G., Ellisman, M. & Fox, D. (2004). The structure-function correlates of mammalian rod and cone photoreceptor mitochondria: Observations and unanswered questions. Mitochondrion 4, 695–703.Google Scholar
Raymond, P. & Barthel, L. (2004). A moving wave patterns the cone photoreceptor mosaic array in the zebrafish retina. The International Journal of Developmental Biology 48, 935–945.Google Scholar
Richardson, K., Jarett, L. & Finke, E. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology 35, 313–323.CrossRefGoogle ScholarPubMed
Robinson, J., Schmitt, E. & Dowling, J. (1995). Temporal and spatial patterns of opsin gene expression in zebrafish (Danio rerio). Visual Neuroscience 12, 895–906.Google Scholar
Robinson, J., Schmitt, E., Harosi, F., Reece, R & Dowling, J. (1993). Zebrafish ultraviolet visual pigment: absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the United States of America 90, 6009–6012.Google Scholar
Sabatini, D., Bensch, K. & Barrnet, R. (1963). Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. The Journal of Cell Biology 17, 19–58.Google Scholar
Saszik, S., Bilotta, J. & Givin, C. (1999). ERG assessment of zebrafish retinal development. Visual Neuroscience 16, 881–888.CrossRefGoogle ScholarPubMed
Schmitt, E., Hyatt, G. & Dowling, J. (1999). Erratum: Temporal and spatial patterns of opsin gene expression in the zebrafish (Danio rerio): Corrections with additions. Visual Neuroscience 16, 601–605.Google Scholar
Sjostrand, F. (1953). The ultrastructure of the inner segments of the retinal rods of the guinea pig eye as revealed by electron microscopy. Journal of Cellular Physiology 42, 45–70.CrossRefGoogle Scholar
Stone, J., van Driel, D., Valter, V., Rees, S. & Provis, J. (2008). The locations of mitochondria in mammalian photoreceptors: Relation to retinal vasculature. Brain Research 1189, 58–69.Google Scholar
Suliman, T. & Novales Flamarique, I. (2014). Visual pigments and opsin expression in the juveniles of three species of fish (rainbow trout, zebrafish, and killifish) following prolonged exposure to thyroid hormone or retinoic acid. The Journal of Comparative Neurology 522, 98–117.Google Scholar
Tarboush, R., Chapman, G. & Connaughton, V. (2012). Ultrastructure of the distal retina of the adult zebrafish, Danio rerio. Tissue Cell 44, 264–279.Google Scholar
Venable, J. & Coggeshall, R. (1965). A simplified lead citrate stain for use in electron microscopy. The Journal of Cell Biology 25, 407–408.Google Scholar
Venkatraman, M., Konga, D., Peramaiyan, R., Ganapathy, E. & Dhanapal, S. (2008). Reduction of mitochondrial oxidative damage and improved mitochondrial efficiency by administration of crocetin against benzo[a]pyrene induced experimental animals. Biological & Pharmaceutical Bulletin 31, 1639–1645.Google Scholar
Vorobyev, M. (2003). Coloured oil droplets enhance colour discrimination. Proceedings. Biological Sciences 270, 1255–1261.Google Scholar
Wong-Riley, M. (2010). Energy metabolism of the visual system. Eye Brain 2, 99–116.Google Scholar
Yamauchi, M., Tsuruma, K., Imai, S., Nakanishi, T., Umigai, N., Shimazawa, M. & Hara, H. (2011). Crocetin prevents retinal degeneration induced by oxidative and endoplasmic reticulum stress via inhibitio of caspase activity. European Journal of Pharmacology 650, 110–119.Google Scholar
Young, S. & Martin, G. (1984). Optics of retinal oil droplets: a model of light collection and polarization detection in the avian retina. Vision Research 24, 129–137.Google Scholar