Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T14:56:54.443Z Has data issue: false hasContentIssue false
  • English
  • Français

Foveolar Müller Cells of the Pied Flycatcher: Morphology and Distribution of Intermediate Filaments Regarding Cell Transparency

Published online by Cambridge University Press:  01 March 2016

Lidia Zueva ,
Tatiana Golubeva ,
Elena Korneeva ,
Vladimir Makarov ,
Igor Khmelinskii Open the ORCID record for Igor Khmelinskii [Opens in a new window]  and
Mikhail Inyushin
Lidia Zueva
Affiliation:
Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, 194223 St-Petersburg, Russia
Tatiana Golubeva
Affiliation:
Department of Vertebrate Zoology, Lomonosov Moscow State University, 119992 Moscow, Russia Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, 117485 Mosсow, Russia
Elena Korneeva
Affiliation:
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, 117485 Mosсow, Russia
Vladimir Makarov
Affiliation:
Department of Physics, University of Puerto Rico, San Juan, PR 00931, USA
Igor Khmelinskii
Affiliation:
Faculty of Sciences and Technology, University of the Algarve, Faro 8005-139, Algarve, Portugal
Mikhail Inyushin*
Affiliation:
Department of Physiology, Central University of the Caribbean, Bayamon, PR 00956, USA
*
*Corresponding author. mikhail.inyushin@uccaribe.edu
Get access

Abstract

Specialized intermediate filaments (IFs) have critical importance for the clearness and uncommon transparency of vertebrate lens fiber cells, although the physical mechanisms involved are poorly understood. Recently, an unusual low-scattering light transport was also described in retinal Müller cells. Exploring the function of IFs in Müller cells, we have studied the morphology and distribution pattern of IFs and other cytoskeletal filaments inside the Müller cell main processes in the foveolar part of the avian (pied flycatcher) retina. We found that some IFs surrounded by globular nanoparticles (that we suggest are crystallines) are present in almost every part of the Müller cells that span the retina, including the microvilli. Unlike IFs implicated in the mechanical architecture of the cell, these IFs are not connected to any specific cellular membranes. Instead, they are organized into bundles, passing inside the cell from the endfeet to the photoreceptor, following the geometry of the processes, and repeatedly circumventing numerous obstacles. We believe that the presently reported data effectively confirm that the model of nanooptical channels built of the IFs may provide a viable explanation of Müller cell transparency.

Keywords

IFsavian retinaMüller cellstransparency
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 2 , April 2016 , pp. 379 - 386
Copyright
© Microscopy Society of America 2016 

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

Agte, S., Junek, S., Matthias, S., Ulbricht, E., Erdmann, I., Wurm, A., Schild, D., Käs, J.A. & Reichenbach, A. (2011). Müller glial cell-provided cellular light guidance through the vital guinea-pig retina. Biophys J 101(11), 2611–2619.CrossRefGoogle ScholarPubMed
Alizadeh, A., Clark, J., Seeberger, T., Hess, J., Blankenship, T. & FitzGerald, P.G. (2003). Targeted deletion of the lens fiber cell-specific intermediate filament protein filensin. Invest Ophthalmol Vis Sci 44, 5252–5258.CrossRefGoogle ScholarPubMed
Alizadeh, A., Clark, J., Seeberger, T., Hess, J., Blankenship, T. & FitzGerald, P.G. (2004). Characterization of a mutation in the lens-specific CP49 in the 129 strain of mouse. Invest Ophthalmol Vis Sci 45(3), 884–891.CrossRefGoogle ScholarPubMed
Alizadeh, A., Clark, J.I., Seeberger, T., Hess, J., Blankenship, T., Spicer, A. & FitzGerald, P.G. (2002). Targeted genomic deletion of the lens-specific intermediate filament protein CP49. Invest Ophthalmol Vis Sci 43(12), 3722–3727.Google Scholar
Benedek, G.B. (1971). Theory of transparency of the eye. Appl Opt 10, 459–471.CrossRefGoogle ScholarPubMed
Bloemendal, H. (1991). Proctor lecture. Disorganisation of membranes and abnormal intermediate filament assembly lead to cataract. Invest Ophthalmol Vis Sci 32, 445–455.Google ScholarPubMed
Cajal, S.R. (1972 [1892]). The Structure of the Retina [translated by S.A. Thorpe & M. Glickstein]. Springfield, IL: Thomas.Google Scholar
Carver, J.A., Aquilina, J.A., Cooper, P.G., Williams, G.A. & Truscott, R.J. (1994). Alpha-crystallin: Molecular chaperone and protein surfactant. Biochim Biophys Acta 1204(2), 195–206.CrossRefGoogle ScholarPubMed
Clark, J.I., Matsushima, H., David, L.L. & Clark, J.M. (1999). Lens cytoskeleton and transparency: A model. Eye (Lond) 13(Pt 3b), 417–424.CrossRefGoogle ScholarPubMed
Delaye, M. & Tardieu, A. (1983). Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302, 415–417.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Harvard University Press.Google Scholar
Fausett, B.V. & Goldman, D. (2006). A role for alpha1 tubulin-expressing Müller glia in regeneration of the injured zebrafish retina. J Neurosci 26(23), 6303–6313.CrossRefGoogle ScholarPubMed
Fischer, A.J., Zelinka, C. & Scott, M.A. (2010). Heterogeneity of glia in the retina and optic nerve of birds and mammals. PLoS One 5(6), e10774.Google Scholar
Franze, K., Grosche, J., Skatchkov, S.N., Schinkinger, S., Foja, C., Schild, D., Uckermann, O., Travis, K., Reichenbach, A. & Guck, J. (2007). Müller cells are living optical fibers in the vertebrate retina. Proc Nat l Acad Sci U S A 104, 8287–8292.CrossRefGoogle Scholar
Jester, J.V. (2008). Corneal crystallins and the development of cellular transparency. Semin Cell Dev Biol 19(2), 82–93.Google Scholar
Johnsen, S. (2001). Hidden in plain sight: The ecology and physiology of organismal transparency. Biol Bull 201(3), 301–318.Google Scholar
Khmelinskii, I., Zueva, L., Inyushin, M. & Makarov, V. (2015). Model of polarization selectivity of the intermediate filament optical channels. Photonics Nanostruct 16, 24–33.Google Scholar
Khokhlova, T.V., Zueva, L.V. & Golubeva, T.B. (2000). Postnatal developmental stages in the retinal photoreceptor cells of Ficedula hypoleuca . Zh Evol Biokhim Fiziol 36, 354–361.Google ScholarPubMed
Kivelä, T., Tarkkanen, A. & Virtanen, I. (1986). Intermediate filaments in the human retina and retinoblastoma. An immunohistochemical study of vimentin, glial fibrillary acidic protein, and neurofilaments. Invest Ophthalmol Vis Sci 27(7), 1075–1084.Google Scholar
Kumar, P.A. & Reddy, G.B. (2009). Modulation of alpha-crystallin chaperone activity: A target to prevent or delay cataract? IUBMB Life 61(5), 485–495.CrossRefGoogle ScholarPubMed
Lewis, G.P., Matsumoto, B. & Fisher, S.K. (1995). Changes in the organization and expression of cytoskeletal proteins during retinal degeneration induced by retinal detachment. Invest Ophthalmol Vis Sci 36(12), 2404–2416.Google Scholar
Makarov, V., Zueva, L., Khmelinskii, I. & Inyushin, M. (2015) On the mechanism of light transmission by Müller cells. arXiv:1503.02923v2 [physics.optics].Google Scholar
Marcantonio, J.M. & Duncan, G. (1991). Calcium-induced degradation of the lens cytoskeleton. Biochem Soc Trans 19, 1148–1150.Google Scholar
Massoudi, D., Malecaze, F. & Galiacy, S.D. (2016). Collagens and proteoglycans of the cornea: Importance in transparency and visual disorders. Cell Tissue Res 363(2), 337–349.CrossRefGoogle ScholarPubMed
Matsushima, H., David, L.L., Hiraoka, T. & Clark, J.I. (1997). Loss of cytoskeletal proteins and lens cell opacification in the selenite cataract model. Exp Eye Res 64, 387–395.Google Scholar
Oka, M., Kudo, H., Sugama, N., Asami, Y. & Takehana, M. (2008). The function of filensin and phakinin in lens transparency. Mol Vis 14, 815–822.Google ScholarPubMed
Perng, M.D., Wen, S.F., Gibbon, T., Middeldorp, J., Sluijs, J., Hol, E.M. & Quinlan, R.A. (2008). Glial fibrillary acidic protein filaments can tolerate the incorporation of assembly-compromised GFAP-delta, but with consequences for filament organization and alphaB-crystallin association. Mol Biol Cell 19(10), 4521–4533.CrossRefGoogle ScholarPubMed
Qu, B., Landsbury, A., Schönthaler, H.B., Dahm, R., Liu, Y., Clark, J.I., Prescott, A.R. & Quinlan, R.A. (2012). Evolution of the vertebrate beaded filament protein, Bfsp2; comparing the in vitro assembly properties of a “tailed” zebrafish Bfsp2 to its “tailless” human orthologue. Exp Eye Res 94(1), 192–202.Google Scholar
Quinlan, R.A., Carte, J.M., Sandilands, A. & Prescott, A.R. (1996). The beaded filament of the eye lens: An unexpected key to intermediate filament structure and function. Trends Cell Biol 6(4), 123–126.Google Scholar
Rafferty, N.S., Rafferty, K.A. & Zigman, S. (1997). Comparative response to UV irradiation of cytoskeletal elements in rabbit and skate lens epithelial cells. Curr Eye Res 16, 310–319.Google Scholar
Reichenbach, A., Hagen, E., Schippel, K. & Eberhardt, W. (1988). Quantitative electron microscopy of rabbit Müller (glial) cells in dependence on retinal topography. Z Mikrosk Anat Forsch 102 (5), 721–755.Google Scholar
Reichenbach, A. & Bridgman, A. (2010). Müller Cells in the Healthy and Diseased Retina, pp. 35–58. Springer, NY, ISBN 978-1-4419-1672-3.Google Scholar
Simirskii, V.N., Panova, I.G., Sologub, A.A. & Aleinikova, K.S. (2003). Localization of crystallins in Mueller cells in the grass frog retina. Ontogenez 34(5), 365–370.Google Scholar
Song, S., Landsbury, A., Dahm, R., Liu, Y., Zhang, Q. & Quinlan, R.A. (2009). Functions of the intermediate filament cytoskeleton in the eye lens. J Clin Invest 119(7), 1837–1848.Google Scholar
Tagliavini, I., Gandolfi, S.A. & Maraini, G. (1986). Cytoskeleton abnormalities in human senile cataract. Curr Eye Res 5, 903–910.Google Scholar
Tardieu, A. & Delaye, M. (1988). Eye lens proteins and transparency: From light transmission theory to solution X-ray structural analysis. Annu Rev Biophys Biophys Chem 17, 47–70.CrossRefGoogle ScholarPubMed
Wakakura, M. & Foulds, W.S. (1988). Comparative ultrastructural study of rabbit Müller cells in vitro and in situ. Eye (Lond) 2(Pt 6), 664–669.CrossRefGoogle ScholarPubMed
Zueva, L., Makarov, V., Zayas-Santiago, A., Golubeva, T., Korneeva, E., Savvinov, A., Eaton, M., Skatchkov, S. & Inyushin, M. (2014). Müller cell alignment in bird fovea: Possible role in vision. J Neurosci Neuroeng 3(2), 85–91.Google Scholar