Rod Photoreceptor Ribbon Synapses in DBA/2J Mice Show Progressive Age-Related Structural Changes

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Fuchs, Michaela ^a   Scholz, Michael ^b   Sendelbeck, Anna ^a   Atorf, Jenny ^c   Schlegel, Christine ^a   Enz, Ralf ^a   Brandstätter, Johann Helmut ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANIMAL TISSUE; ARTICLE; CLOSED ANGLE GLAUCOMA; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRON MICROSCOPY; MOUSE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; RETINA DEGENERATION; RETINA ROD; ROD PHOTORECEPTOR RIBBON SYNAPSE; SYNAPSE; UPREGULATION;

AGING; ANIMALS; COMPLEMENT C1Q; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; GLAUCOMA; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICROSCOPY, ELECTRON; OPTIC NERVE; PHENOTYPE; RETINAL GANGLION CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SPECIES SPECIFICITY; SYNAPSES; TIME FACTORS;

ANIMALIA; MUS;

EID: 84866015157     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044645     Document Type: Article

References (36)

1. John SW, Smith RS, Savinova OV, Hawes NL, Chang B, et al. (1998) Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice. Invest Ophthalmol Vis Sci 39 (6): 951-962.
2. Libby RT, Anderson MG, Pang IH, Robinson ZH, Savinova OV, et al. (2005) Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration. Vis Neurosci 22 (5): 637-648.
3. Scholz M, Buder T, Seeber S, Adamek E, Becker CM, et al. (2008) Dependency of intraocular pressure elevation and glaucomatous changes in DBA/2J and DBA/2J-Rj mice. Invest Ophthalmol Vis Sci 49 (2): 613-621.
4. John SWM, (2005) Mechanistic insights into glaucoma provided by experimental genetics. The Cogan Lecture. Invest. Ophthalmol Vis Sci 46 (8): 2649-2661.
5. Moon JI, Kim IB, Gwon JS, Park MH, Kang TH, et al. (2005) Changes in retinal neuronal populations in the DBA/2J mouse. Cell Tissue Res 320 (1): 51-59.
6. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson EDO, et al. (2008) Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J Neurosci 28 (2): 548-561.
7. Danias J, Lee KC, Zamora MF, Chen B, Shen F, et al. (2003) Quantitative analysis of retinal ganglion cell (RGC) loss in aging DBA/2NNia glaucomatous mice: comparison with RGC loss in aging C57/BL6 mice. Invest Ophthalmol Vis Sci 44 (12): 5151-5162.
8. Jakobs TC, Libby RT, Ben Y, John SWM, Masland RH, (2005) Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol 171 (2): 313-325.
9. Birke MT, Neumann C, Birke K, Kremers J, Scholz M, (2010) Changes of osteopontin in the aqueous humor of the DBA2/J glaucoma model correlated with optic nerve and RGC degenerations. Invest Ophthalmol Vis Sci 51 (11): 5759-5767.
10. Harazny J, Scholz M, Buder T, Lausen B, Kremers J, (2009) Electrophysiological deficits in the retina of the DBA/2J mouse. Doc Ophthalmol 119 (3): 181-197.
11. Heiduschka P, Julien S, Schuettauf F, Schnichels S, (2010) Loss of retinal function in aged DBA/2J mice- New insights into retinal neurodegeneration. Exp Eye Res 91 (5): 779-783.
12. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, et al. (2005) Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168 (5): 825-836.
13. tom Dieck S, Brandstätter JH, (2006) Ribbon synapses of the retina. Cell Tissue Res 326 (2): 339-346.
14. Schmitz F, Königstorfer A, Südhof TC, (2000) RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28 (3): 857-872.
15. Dick O, tom Dieck S, Altrock WD, Ammermüller J, Weiler R, et al. (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37 (5): 775-786.
16. Stasi K, Nagel D, Yang X, Wang RF, Ren L, et al. (2006) Complement component 1Q (C1Q) upregulation in retina of murine, primate, and human glaucomatous eyes. Invest Ophthalmol Vis Sci 47 (3): 1024-1029.
17. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, et al. (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131 (6): 1164-1178.
18. Regus-Leidig H, Specht D, tom Dieck S, Brandstätter JH, (2010) Stability of active zone components at the photoreceptor ribbon complex. Mol Vis 16: 2690-2700.
19. Blanks JC, Adinolfi AM, Lolley RN, (1974) Synaptogenesis in the photoreceptor terminal of the mouse retina. J Comp Neurol 156 (1): 81-93.
20. Regus-Leidig H, tom Dieck S, Specht D, Meyer L, Brandstätter JH, (2009) Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: the involvement of precursor spheres. J Comp Neurol 512 (6): 814-824.
21. Regus-Leidig H, tom Dieck S, Brandstätter JH, (2010) Absence of functional active zone protein Bassoon affects assembly and transport of ribbon precursors during early steps of photoreceptor synaptogenesis. Eur J Cell Biol 89 (6): 468-475.
22. Haeseleer F, Imanishi Y, Maeda T, Possin DE, Maeda A, et al. (2004) Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7 (10): 1079-1087.
23. Grossman GH, Pauer GJ, Narendra U, Peachey NS, Hagstrom SA, (2009) Early synaptic defects in tulp1-/- mice. Invest Ophthalmol Vis Sci 50 (7): 3074-3083.
24. Reim K, Regus-Leidig H, Ammermüller J, El-Kordi A, Radyushkin K, et al. (2009) Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4. J Cell Sci 122 (9): 1352-1361.
25. Frishman LJ (2006) Origins of the electroretinogram. In: Heckenlively JR, Arden GB, editors. Principles and practice of clinical electrophysiology of vision. Cambridge, Mass: MIT Press. 139-183.
26. Dyka FM, May CA, Enz R, (2004) Metabotropic glutamate receptors are differentially regulated under elevated intraocular pressure. J Neurochem 90 (1): 190-202.
27. Huang W, Xing W, Ryskamp DA, Punzo C, Križaj D, (2011) Localization and phenotype-specific expression of ryanodine calcium release channels in C57BL6 and DBA/2J mouse strains. Exp Eye Res 93 (5): 700-709.
28. Dyka FM, May CA, Enz R, (2005) Subunits of the epithelial sodium channel family are differentially expressed in the retina of mice with ocular hypertension. J Neurochem 94 (1): 120-128.
29. Howell GR, Macalinao DG, Sousa GL, Walden M, Soto I, et al. (2011) Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J Clin Invest 121 (4): 1429-1444.
30. Perry VH, O'Connor V, (2008) C1q: the perfect complement for a synaptic feast. Nat Rev Neurosci 9 (11): 807-811.
31. Panagis L, Zhao X, Ge Y, Ren L, Mittag TW, et al. (2011) Retinal gene expression changes related to IOP exposure and axonal loss in DBA/2J mice. Invest Ophthalmol Vis Sci 52 (11): 7807-7816.
32. Steele MR, Inman DM, Calkins DJ, Horner PJ, Vetter ML, (2006) Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest Ophthalmol Vis Sci 47 (3): 977-985.
33. Chang B, Smith RS, Hawes NL, Anderson MG, Zabaleta A, et al. (1999) Interacting loci cause severe iris atrophy and glaucoma in DBA/2J mice. Nat Genet 21 (4): 405-409.
34. Haverkamp S, Wässle H, (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424 (1): 1-23.
35. Haeseleer F, Sokal I, Verlinde CL, Erdjument-Bromage H, Tempst P, et al. (2000) Five members of a novel Ca2+-binding protein (CABP) subfamily with similarity to calmodulin. J Biol Chem 275 (2): 1247-1260.
36. Specht D, Wu SB, Turner P, Dearden P, Koentgen F, et al. (2009) Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Invest Ophthalmol Vis Sci 50 (2): 505-515.