Activation of survival pathways in the degenerating retina of rd10 mice

Experimental Eye Research

Volumn 99, Issue 1, 2012, Pages 17-26

  Samardzija, Marijana ^a   Wariwoda, Hedwig ^a   Imsand, Cornelia ^a   Huber, Philipp ^a   Heynen, Severin R ^a   Gubler, Andrea ^a   Grimm, Christian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Leukemia inhibitory factor; LIF; Photoreceptor degeneration; Rd10; Retina; Signaling; Vasculature

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CEBPD PROTEIN; EDN2 PROTEIN; FIBROBLAST GROWTH FACTOR 2; LIF PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL DEATH; CONTROLLED STUDY; DISEASE COURSE; GENE EXPRESSION; IMMUNOFLUORESCENCE; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RETINA CONE; RETINA DEGENERATION; RETINA ROD; SIGNAL TRANSDUCTION; SURVIVAL PATHWAY ACTIVATION; WESTERN BLOTTING;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; ATROPHY; BLOTTING, WESTERN; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENDOTHELIN-2; FIBROBLAST GROWTH FACTOR 2; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; IN SITU NICK-END LABELING; LEUKEMIA INHIBITORY FACTOR; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PHOTORECEPTOR CELLS, VERTEBRATE; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; RETINAL VESSELS; SIGNAL TRANSDUCTION;

EID: 84861690239     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.04.004     Document Type: Article

References (49)

1. Applebury M.L., Antoch M.P., Baxter L.C., Chun L.L., Falk J.D., Farhangfar F., Kage K., Krzystolik M.G., Lyass L.A., Robbins J.T. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 2000, 27:513-523.
2. Balamurugan K., Wang J.M., Tsai H.H., Sharan S., Anver M., Leighty R., Sterneck E. The tumour suppressor C/EBPdelta inhibits FBXW7 expression and promotes mammary tumour metastasis. EMBO J. 2010, 29:4106-4117.
3. Barhoum R., Martinez-Navarrete G., Corrochano S., Germain F., Fernandez-Sanchez L., de la Rosa E.J., de la Villa P., Cuenca N. Functional and structural modifications during retinal degeneration in the rd10 mouse. Neuroscience 2008, 155:698-713.
4. Blasiak J., Szaflik J., Szaflik J.P. Implications of altered iron homeostasis for age-related macular degeneration. Front. Biosci. 2011, 16:1551-1559.
5. Bowes C., Li T., Danciger M., Baxter L.C., Applebury M.L., Farber D.B. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 1990, 347:677-680.
6. Burgi S., Samardzija M., Grimm C. Endogenous leukemia inhibitory factor protects photoreceptor cells against light-induced degeneration. Mol. Vis. 2009, 15:1631-1637.
7. Caprara C., Thiersch M., Lange C., Joly S., Samardzija M., Grimm C. HIF1A is essential for the development of the intermediate plexus of the retinal vasculature. Invest. Ophthalmol. Vis. Sci. 2011, 52:2109-2117.
8. Chang B., Hawes N.L., Pardue M.T., German A.M., Hurd R.E., Davisson M.T., Nusinowitz S., Rengarajan K., Boyd A.P., Sidney S.S., Phillips M.J., Stewart R.E., Chaudhury R., Nickerson J.M., Heckenlively J.R., Boatright J.H. Two mouse retinal degenerations caused by missense mutations in the beta-subunit of rod cGMP phosphodiesterase gene. Vision Res. 2007, 47:624-633.
9. Chen J.J., Huang W.C., Chen C.C. Transcriptional regulation of cyclooxygenase-2 in response to proteasome inhibitors involves reactive oxygen species-mediated signaling pathway and recruitment of CCAAT/enhancer-binding protein delta and CREB-binding protein. Mol. Biol. Cell. 2005, 16:5579-5591.
10. Chin M.S., Nagineni C.N., Hooper L.C., Detrick B., Hooks J.J. Cyclooxygenase-2 gene expression and regulation in human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 2001, 42:2338-2346.
11. Chollangi S., Wang J., Martin A., Quinn J., Ash J.D. Preconditioning-induced protection from oxidative injury is mediated by leukemia inhibitory factor receptor (LIFR) and its ligands in the retina. Neurobiol. Dis. 2009, 34:535-544.
12. Deleon E., Lederman M., Berenstein E., Meir T., Chevion M., Chowers I. Alteration in iron metabolism during retinal degeneration in rd10 mouse. Invest. Ophthalmol. Vis. Sci. 2009, 50:1360-1365.
13. Dong A., Shen J., Krause M., Akiyama H., Hackett S.F., Lai H., Campochiaro P.A. Superoxide dismutase 1 protects retinal cells from oxidative damage. J. Cell Physiol. 2006, 208:516-526.
14. Doonan F., O'Driscoll C., Kenna P., Cotter T.G. Enhancing survival of photoreceptor cells in vivo using the synthetic progestin norgestrel. J. Neurochem. 2011, 118:915-927.
15. Farber D.B., Lolley R.N. Cyclic guanosine monophosphate: elevation in degenerating photoreceptor cells of the C3H mouse retina. Science 1974, 186:449-451.
16. Gargini C., Terzibasi E., Mazzoni F., Strettoi E. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J. Comp. Neurol. 2007, 500:222-238.
17. Guo Y., Cepurna W.O., Dyck J.A., Doser T.A., Johnson E.C., Morrison J.C. Retinal cell responses to elevated intraocular pressure: a gene array comparison between the whole retina and retinal ganglion cell layer. Invest. Ophthalmol. Vis. Sci. 2010, 51:3003-3018.
18. Guo Y., Johnson E.C., Cepurna W.O., Dyck J.A., Doser T., Morrison J.C. Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 2011, 52:1460-1473.
19. Hafezi F., Steinbach J.P., Marti A., Munz K., Wang Z.Q., Wagner E.F., Aguzzi A., Reme C.E. The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat. Med. 1997, 3:346-349.
20. Haverkamp S., Wassle H., Duebel J., Kuner T., Augustine G.J., Feng G., Euler T. The primordial, blue-cone color system of the mouse retina. J. Neurosci. 2005, 25:5438-5445.
21. Hour T.C., Lai Y.L., Kuan C.I., Chou C.K., Wang J.M., Tu H.Y., Hu H.T., Lin C.S., Wu W.J., Pu Y.S., Sterneck E., Huang A.M. Transcriptional up-regulation of SOD1 by CEBPD: a potential target for cisplatin resistant human urothelial carcinoma cells. Biochem. Pharmacol. 2010, 80:325-334.
22. Jaliffa C., Ameqrane I., Dansault A., Leemput J., Vieira V., Lacassagne E., Provost A., Bigot K., Masson C., Menasche M., Abitbol M. Sirt1 involvement in rd10 mouse retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2009, 50:3562-3572.
23. Joly S., Lange C., Thiersch M., Samardzija M., Grimm C. Leukemia inhibitory factor extends the lifespan of injured photoreceptors in vivo. J. Neurosci. 2008, 28:13765-13774.
24. Kinoshita S., Akira S., Kishimoto T. A member of the C/EBP family, NF-IL6 beta, forms a heterodimer and transcriptionally synergizes with NF-IL6. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:1473-1476.
25. Ko C.Y., Chang L.H., Lee Y.C., Sterneck E., Cheng C.P., Chen S.H., Huang A.M., Tseng J.T., Wang J.M. CCAAT/enhancer binding protein delta (CEBPD) elevating PTX3 expression inhibits macrophage-mediated phagocytosis of dying neuron cells. Neurobiol. Aging 2012, 33:422.e11-422.e25.
26. Ko C.Y., Hsu H.C., Shen M.R., Chang W.C., Wang J.M. Epigenetic silencing of CCAAT/enhancer-binding protein delta activity by YY1/polycomb group/DNA methyltransferase complex. J. Biol. Chem. 2008, 283:30919-30932.
27. Lange C., Heynen S.R., Tanimoto N., Thiersch M., Le Y.Z., Meneau I., Seeliger M.W., Samardzija M., Caprara C., Grimm C. Normoxic activation of hypoxia-inducible factors in photoreceptors provides transient protection against light-induced retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2011, 52:5872-5880.
28. Malaspina A., Ngoh S.F., Ward R.E., Hall J.C., Tai F.W., Yip P.K., Jones C., Jokic N., Averill S.A., Michael-Titus A.T., Priestley J.V. Activation transcription factor-3 activation and the development of spinal cord degeneration in a rat model of amyotrophic lateral sclerosis. Neuroscience 2010, 169:812-827.
29. Obolensky A., Berenshtein E., Lederman M., Bulvik B., Alper-Pinus R., Yaul R., Deleon E., Chowers I., Chevion M., Banin E. Zinc-desferrioxamine attenuates retinal degeneration in the rd10 mouse model of Retinitis Pigmentosa. Free Radic. Biol. Med. 2011, 51:1482-1491.
30. Otani A., Dorrell M.I., Kinder K., Moreno S.K., Nusinowitz S., Banin E., Heckenlively J., Friedlander M. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J. Clin. Invest. 2004, 114:765-774.
31. Phillips M.J., Otteson D.C., Sherry D.M. Progression of neuronal and synaptic remodeling in the rd10 mouse model of Retinitis Pigmentosa. J. Comp. Neurol. 2010, 518:2071-2089.
32. Picard E., Ranchon-Cole I., Jonet L., Beaumont C., Behar-Cohen F., Courtois Y., Jeanny J.C. Light-induced retinal degeneration correlates with changes in iron metabolism gene expression, ferritin level, and aging. Invest. Ophthalmol. Vis. Sci. 2011, 52:1261-1274.
33. Piehl L., Capani F., Facorro G., Lopez E.M., de Celis E.R., Pustovrh C., Hager A., Coirini H., Lopez-Costa J.J. Nitric oxide increases in the rat retina after continuous illumination. Brain Res. 2007, 1156:112-119.
34. Portera-Cailliau C., Sung C.H., Nathans J., Adler R. Apoptotic photoreceptor cell death in mouse models of Retinitis Pigmentosa. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:974-978.
35. Prasad S.S., Kojic L., Wen Y.H., Chen Z., Xiong W., Jia W., Cynader M.S. Retinal gene expression after central retinal artery ligation: effects of ischemia and reperfusion. Invest. Ophthalmol. Vis. Sci. 2010, 51:6207-6219.
36. Rex T.S., Allocca M., Domenici L., Surace E.M., Maguire A.M., Lyubarsky A., Cellerino A., Bennett J., Auricchio A. Systemic but not intraocular Epo gene transfer protects the retina from light-and genetic-induced degeneration. Mol. Ther. 2004, 10:855-861.
37. Samardzija M., Neuhauss S.C.F., Joly S., Kurz-Levin M., Grimm C. Animal models for retinal degeneration. Animal Models Retin. Dis. 2010, 46:51-79.
38. Samardzija M., Wenzel A., Aufenberg S., Thiersch M., Reme C., Grimm C. Differential role of Jak-STAT signaling in retinal degenerations. FASEB J. 2006, 20:2411-2413.
39. Samardzija M., Wenzel A., Thiersch M., Frigg R., Reme C., Grimm C. Caspase-1 ablation protects photoreceptors in a model of autosomal dominant Retinitis Pigmentosa. Invest. Ophthalmol. Vis. Sci. 2006, 47:5181-5190.
40. Thiersch M., Raffelsberger W., Frigg R., Samardzija M., Wenzel A., Poch O., Grimm C. Analysis of the retinal gene expression profile after hypoxic preconditioning identifies candidate genes for neuroprotection. BMC Genomics 2008, 9:73.
41. Thompson M.R., Xu D., Williams B.R. ATF3 transcription factor and its emerging roles in immunity and cancer. J. Mol. Med. (Berl.) 2009, 87:1053-1060.
42. Ueki Y., Wang J., Chollangi S., Ash J.D. STAT3 activation in photoreceptors by leukemia inhibitory factor is associated with protection from light damage. J. Neurochem. 2008, 105:784-796.
43. Wenzel A., Grimm C., Marti A., Kueng-Hitz N., Hafezi F., Niemeyer G., Reme C.E. c-fos controls the "private pathway" of light-induced apoptosis of retinal photoreceptors. J. Neurosci. 2000, 20:81-88.
44. Wunderlich K.A., Leveillard T., Penkowa M., Zrenner E., Perez M.T. Altered expression of metallothionein-I and -II and their receptor megalin in inherited photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci. 2010, 51:4809-4820.
45. Yang L.P., Li Y., Zhu X.A., Tso M.O. Minocycline delayed photoreceptor death in rds mice through iNOS-dependent mechanism. Mol. Vis. 2007, 13:1073-1082.
46. Yanni S.E., McCollum G.W., Penn J.S. Genetic deletion of COX-2 diminishes VEGF production in mouse retinal Muller cells. Exp. Eye Res. 2010, 91:34-41.
47. Yin J., Thomas F., Lang J.C., Chaum E. Modulation of oxidative stress responses in the human retinal pigment epithelium following treatment with vitamin C. J. Cell Physiol. 2011, 226:2025-2032.
48. Zhang T., Zhang N., Baehr W., Fu Y. Cone opsin determines the time course of cone photoreceptor degeneration in Leber congenital amaurosis. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8879-8884.
49. Zigmond R.E., Vaccariello S.A. Activating transcription factor 3 immunoreactivity identifies small populations of axotomized neurons in rat cervical sympathetic ganglia after transection of the preganglionic cervical sympathetic trunk. Brain Res. 2007, 1159:119-123.