Photoreceptor cell death, proliferation and formation of hybrid rod/S-cone photoreceptors in the degenerating STK38L mutant retina

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Berta, Ágnes I ^a,b   Boesze Battaglia, Kathleen ^a   Genini, Sem ^a   Goldstein, Orly ^c   O'Brien, Paul J ^d   Szél, Ágoston ^b   Acland, Gregory M ^c   Beltran, William A ^a   Aguirre, Gustavo D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^c Department of Obstetrics Gynecology   (United States)

^d NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD18 ANTIGEN; CELL PROTEIN; CYCLIN A1; GLUTAMATE AMMONIA LIGASE; LONG ACTING THYROID STIMULATOR; NESTIN; OPSIN; PROTEIN CRX; PROTEIN NR2E3; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; GLUTAMINE; INTERMEDIATE FILAMENT PROTEIN; NERVE PROTEIN; PROTEIN SERINE THREONINE KINASE; SCOTOPSIN; STK38L PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOG; GENE; GENE MUTATION; MACROPHAGE; MICROGLIA; MUELLER CELL; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NICK END LABELING; NONHUMAN; PHOTORECEPTOR CELL; PHOTORECEPTOR OUTER SEGMENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA CONE; RETINA DEGENERATION; RETINA ROD; STK38L GENE; UPREGULATION; VISUAL SYSTEM DEVELOPMENT; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; KINETICS; METABOLISM; METHODOLOGY; MUTATION; RETINA;

CANIS FAMILIARIS;

ANIMALS; CELL PROLIFERATION; DOGS; GENE EXPRESSION REGULATION; GLUTAMINE; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT PROTEINS; KINETICS; MODELS, BIOLOGICAL; MUTATION; NERVE TISSUE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RETINA; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; ROD OPSINS;

EID: 80053618314     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024074     Document Type: Article

References (40)

1. Aguirre GD, Acland GM, (2006) Models, Mutants and Man: Searching for Unique Phenotypes and genes in the Dog Model of Inherited Retinal Degeneration. In: Ostrander EA, Giger U, Lindblad-Toh K, editors. The Dog and Its Genome Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press pp. 291-325.
2. Baehr W, Frederick JM, (2009) Naturally occurring animal models with outer retina phenotypes. Vision Res 49: 2636-2652.
3. Portera-Cailliau C, Sung CH, Nathans J, Adler R, (1994) Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. Proc Natl Acad Sci U S A 91: 974-978.
4. Doonan F, Donovan M, Cotter TG, (2005) Activation of multiple pathways during photoreceptor apoptosis in the rd mouse. Invest Ophthalmol Vis Sci 46: 3530-3538.
5. Lohr HR, Kuntchithapautham K, Sharma AK, Rohrer B, (2006) Multiple, parallel cellular suicide mechanisms participate in photoreceptor cell death. Exp Eye Res 83: 380-389.
6. Acland GM, Aguirre GD, (1987) Retinal degenerations in the dog: IV. Early retinal degeneration (erd) in Norwegian elkhounds. Experimental Eye Research 44: 491-521.
7. Goldstein O, Kukekova AV, Aguirre GD, Acland GM, (2010) Exonic SINE insertion in STK38L causes canine early retinal degeneration (erd). Genomics 96: 362-368.
8. Hergovich A, Stegert MR, Schmitz D, Hemmings BA, (2006) NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol 7: 253-264.
9. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S, (2002) The protein kinase complement of the human genome. Science 298: 1912-1934.
10. Akhmedov NB, Yamashita CK, Tran D, Piri NI, Aguirre GD, et al. (2005) Two forms of the large tumor suppressor gene (Lats1) protein expressed in the vertebrate retina. Biochim Biophys Acta 1728: 11-17.
11. Beltran WA, Hammond P, Acland GM, Aguirre GD, (2006) A frameshift mutation in RPGR exon ORF15 causes photoreceptor degeneration and inner retina remodeling in a model of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci 47: 1669-1681.
12. Hans F, Dimitrov S, (2001) Histone H3 phosphorylation and cell division. Oncogene 20: 3021-3027.
13. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, et al. (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235-239.
14. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, et al. (2005) Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 25: 9350-9359.
15. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ, et al. (2000) Retinal stem cells in the adult mammalian eye. Science 287: 2032-2036.
16. Rohlich P, Szel A, (1993) Binding sites of photoreceptor-specific antibodies COS-1, OS-2 and AO. Curr Eye Res 12: 935-944.
17. Swaroop A, Kim D, Forrest D, (2010) Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina. Nat Rev Neurosci 11: 563-576.
18. Beltran WA, Wen R, Acland GM, Aguirre GD, (2007) Intravitreal injection of ciliary neurotrophic factor (CNTF) causes peripheral remodeling and does not prevent photoreceptor loss in canine RPGR mutant retina. Exp Eye Res 84: 753-771.
19. Mowat FM, Petersen-Jones SM, Williamson H, Williams DL, Luthert PJ, et al. (2008) Topographical characterization of cone photoreceptors and the area centralis of the canine retina. Mol Vis 14: 2518-2527.
20. Belvindrah R, Rougon G, Chazal G, (2002) Increased neurogenesis in adult mCD24-deficient mice. J Neurosci 22: 3594-3607.
21. Luzzati F, De Marchis S, Fasolo A, Peretto P, (2006) Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26: 609-621.
22. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, et al. (2008) Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A 105: 19508-19513.
23. Lamba D, Karl M, Reh T, (2008) Neural regeneration and cell replacement: a view from the eye. Cell Stem Cell 2: 538-549.
24. Montgomery JE, Parsons MJ, Hyde DR, (2010) A novel model of retinal ablation demonstrates that the extent of rod cell death regulates the origin of the regenerated zebrafish rod photoreceptors. J Comp Neurol 518: 800-814.
25. Menu dit Huart L, Lorentz O, Goureau O, Leveillard T, Sahel JA, (2004) DNA repair in the degenerating mouse retina. Mol Cell Neurosci 26: 441-449.
26. Zeiss CJ, Johnson EA, (2004) Proliferation of microglia, but not photoreceptors, in the outer nuclear layer of the rd-1 mouse. Invest Ophthalmol Vis Sci 45: 971-976.
27. al-Ubaidi MR, Hollyfield JG, Overbeek PA, Baehr W, (1992) Photoreceptor degeneration induced by the expression of simian virus 40 large tumor antigen in the retina of transgenic mice. Proc Natl Acad Sci U S A 89: 1194-1198.
28. Oh EC, Cheng H, Hao H, Jia L, Khan NW, et al. (2008) Rod differentiation factor NRL activates the expression of nuclear receptor NR2E3 to suppress the development of cone photoreceptors. Brain Res 1236: 16-29.
29. Corbo JC, Cepko CL, (2005) A hybrid photoreceptor expressing both rod and cone genes in a mouse model of enhanced S-cone syndrome. PLoS Genet 1: e11.
30. Cheng H, Khanna H, Oh EC, Hicks D, Mitton KP, et al. (2004) Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors. Hum Mol Genet 13: 1563-1575.
31. Peng GH, Ahmad O, Ahmad F, Liu J, Chen S, (2005) The photoreceptor-specific nuclear receptor Nr2e3 interacts with Crx and exerts opposing effects on the transcription of rod versus cone genes. Hum Mol Genet 14: 747-764.
32. Young RW, (1969) A difference between rods and cones in the renewal of outer segment protein. Invest Ophthalmol 8: 222-231.
33. Liebman PA, Entine G, (1974) Lateral diffusion of visual pigment in photoreceptor disk membranes. Science 185: 457-459.
34. Aguirre G, O'Brien P, (1986) Morphological and biochemical studies of canine progressive rod-cone degeneration. 3H-fucose autoradiography. Invest Ophthalmol Vis Sci 27: 635-655.
35. LaVail MM, (1976) Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science 194: 1071-1074.
36. Conley SM, Stricker HM, Naash MI, (2010) Biochemical analysis of phenotypic diversity associated with mutations in codon 244 of the retinal degeneration slow gene. Biochemistry 49: 905-911.
37. Oh EC, Khan N, Novelli E, Khanna H, Strettoi E, et al. (2007) Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proc Natl Acad Sci U S A 104: 1679-1684.
38. Zhang Q, Acland GM, Wu WX, Johnson JL, Pearce-Kelling S, et al. (2002) Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration. Human Molecular Genetics 11: 993-1003.
39. Szel A, Takacs L, Monostori E, Diamantstein T, Vigh-Teichmann I, et al. (1986) Monoclonal antibody-recognizing cone visual pigment. Exp Eye Res 43: 871-883.
40. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.