Retina-specific activation of a sustained hypoxia-like response leads to severe retinal degeneration and loss of vision

Neurobiology of Disease

Volumn 41, Issue 1, 2011, Pages 119-130

  Lange, Christina ^a   Caprara, Christian ^a   Tanimoto, Naoyuki ^b   Beck, Susanne ^b   Huber, Gesine ^b   Samardzija, Marijana ^a   Seeliger, Mathias ^b   Grimm, Christian ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Centre for Ophthalmology   (Germany)

Author keywords

Caspase; HIF; Photoreceptor; Retina; Retinal degeneration; Vasculature; Von Hippel Lindau

Indexed keywords

CASPASE 3; CASPASE 8; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 2; INTERLEUKIN 1BETA CONVERTING ENZYME; LEUKEMIA INHIBITORY FACTOR; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME INDUCTION; EXTRACELLULAR MATRIX; GENE CONTROL; GENE TARGETING; IRIS; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PATHOGENESIS; PHOTORECEPTOR; POSTERIOR EYE CHAMBER; PRIORITY JOURNAL; RETINA BLOOD FLOW; RETINA DEGENERATION; RETINA NERVE CELL; TRANSCRIPTION INITIATION; VASCULAR DISEASE; VISUAL IMPAIRMENT;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLINDNESS; CELL DEATH; CELL SURVIVAL; DISEASE MODELS, ANIMAL; HYPOXIA, BRAIN; HYPOXIA-INDUCIBLE FACTOR 1; LEUKEMIA INHIBITORY FACTOR; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; RETINAL ARTERY; RETINAL DEGENERATION; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 78349305123     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.08.028     Document Type: Article

References (51)

1. Ahmed A.A., Mills A.D., Ibrahim A.E., Temple J., Blenkiron C., Vias M., Massie C.E., Iyer N.G., McGeoch A., Crawford R., Nicke B., Downward J., Swanton C., Bell S.D., Earl H.M., Laskey R.A., Caldas C., Brenton J.D. The extracellular matrix protein TGFBI induces microtubule stabilization and sensitizes ovarian cancers to paclitaxel. Cancer Cell 2007, 12:514-527.
2. 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.
3. Barnstable C.J., Tombran-Tink J. Neuroprotective and antiangiogenic actions of PEDF in the eye: molecular targets and therapeutic potential. Prog. Retin. Eye Res. 2004, 23:561-577.
4. Biju M.P., Neumann A.K., Bensinger S.J., Johnson R.S., Turka L.A., Haase V.H. Vhlh gene deletion induces Hif-1-mediated cell death in thymocytes. Mol. Cell. Biol. 2004, 24:9038-9047.
5. Bishop T., Lau K.W., Epstein A.C., Kim S.K., Jiang M., O'Rourke D., Pugh C.W., Gleadle J.M., Taylor M.S., Hodgkin J., Ratcliffe P.J. Genetic analysis of pathways regulated by the von Hippel-Lindau tumor suppressor in Caenorhabditis elegans. PLoS Biol. 2004, 2:e289.
6. Braun R.D., Linsenmeier R.A. Retinal oxygen tension and the electroretinogram during arterial occlusion in the cat. Invest. Ophthalmol. Vis. Sci. 1995, 36:523-541.
7. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 1999, 15:269-290.
8. Burgi S., Samardzija M., Grimm C. Endogenous leukemia inhibitory factor protects photoreceptor cells against light-induced degeneration. Mol. Vis. 2009, 15:1631-1637.
9. Bustamante M., Tasinato A., Maurer F., Elkochairi I., Lepore M.G., Arsenijevic Y., Pedrazzini T., Munier F.L., Schorderet D.F. Overexpression of a mutant form of TGFBI/BIGH3 induces retinal degeneration in transgenic mice. Mol. Vis. 2008, 14:1129-1137.
10. 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.
11. Doonan F., Donovan M., Cotter T.G. Caspase-independent photoreceptor apoptosis in mouse models of retinal degeneration. J. Neurosci. 2003, 23:5723-5731.
12. Fischer M.D., Huber G., Beck S.C., Tanimoto N., Muehlfriedel R., Fahl E., Grimm C., Wenzel A., Reme C.E., van de Pavert S.A., Wijnholds J., Pacal M., Bremner R., Seeliger M.W. Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography. PLoS One 2009, 4:e7507.
13. Fruttiger M. Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest. Ophthalmol. Vis. Sci. 2002, 43:522-527.
14. Grimm C., Wenzel A., Groszer M., Mayser H., Seeliger M., Samardzija M., Bauer C., Gassmann M., Reme C.E. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat. Med. 2002, 8:718-724.
15. Grimm C., Hermann D.M., Bogdanova A., Hotop S., Kilic U., Wenzel A., Kilic E., Gassmann M. Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin. Cell Dev. Biol. 2005, 16:531-538.
16. Grimm C., Wenzel A., Acar N., Keller S., Seeliger M., Gassmann M. Hypoxic preconditioning and erythropoietin protect retinal neurons from degeneration. Adv. Exp. Med. Biol. 2006, 588:119-131.
17. Guicciardi M.E., Gores G.J. Life and death by death receptors. FASEB J. 2009, 23:1625-1637.
18. Haase V.H., Glickman J.N., Socolovsky M., Jaenisch R. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1583-1588.
19. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7987-7992.
20. Huber G., Beck S.C., Grimm C., Sahaboglu-Tekgoz A., Paquet-Durand F., Wenzel A., Humphries P., Redmond T.M., Seeliger M.W., Fischer M.D. Spectral domain optical coherence tomography in mouse models of retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2009, 50:5888-5895.
21. Iriyogen M., Pajares M.J., Agorreta J., Ponz-Sarvise M., Salvo E., Lozano M.D., Pio R., Gil-Bazo I., Rouzaut A. TGFBI expression is associated with a better response to chemotherapy in NSCLC. Mol. Cancer 2010, 9:130.
22. Ito M., Yoshioka M. Regression of the hyaloid vessels and pupillary membrane of the mouse. Anat. Embryol. (Berl.) 1999, 200:403-411.
23. 2 sensing. Science 2001, 292:464-468.
24. Ivanov S.V., Ivanova A.V., Salnikow K., Timofeeva O., Subramaniam M., Lerman M.I. Two novel VHL targets, TGFBI (BIGH3) and its transactivator KLF10, are up-regulated in renal clear cell carcinoma and other tumors. Biochem. Biophys. Res. Commun. 2008, 370:536-540.
25. Iwai K., Yamanaka K., Kamura T., Minato N., Conaway R.C., Conaway J.W., Klausner R.D., Pause A. Identification of the von Hippel-Lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:12436-12441.
26. 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.
27. Jomary C., Neal M.J., Jones S.E. Characterization of cell death pathways in murine retinal neurodegeneration implicates cytochrome c release, caspase activation, and bid cleavage. Mol. Cell. Neurosci. 2001, 18:335-346.
28. Kamura T., Koepp D.M., Conrad M.N., Skowyra D., Moreland R.J., Iliopoulos O., Lane W.S., Kaelin W.G., Elledge S.J., Conaway R.C., Harper J.W., Conaway J.W. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 1999, 284:657-661.
29. Kibel A., Iliopoulos O., DeCaprio J.A., Kaelin W.G. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C. Science 1995, 269:1444-1446.
30. Kurihara T., Kubota Y., Ozawa Y., Takubo Y., Noda K., Simon M.C., Johnson R.S., Suematsu M., Tsubota K., Ishida K., Goda N., Suda T., Okano H. von Hippel-Lindau protein regulates transition from the fetal to the adult circulatory system in retina. Development 2010, 137:1563-1571.
31. Lee S., Nakamura E., Yang H., Wei W., Linggi M.S., Sajan M.P., Farese R.V., Freeman R.S., Carter B.D., Kaelin W.G., Schlisio S. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 2005, 8:155-167.
32. Ma C., Rong Y., Radiloff D.R., Datto M.B., Centeno B., Bao S., Cheng A.W., Lin F., Jiang S., Yeatman T.J., Wang X.F. Extracellular matrix protein betaig-h3/TGFBI promotes metastasis of colon cancer by enhancing cell extravasation. Genes Dev. 2008, 22:308-321.
33. Marquardt T., Ashery-Padan R., Andrejewski N., Scardigli R., Guillemot F., Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 2001, 105:43-55.
34. O'Driscoll C., Donovan M., Cotter T.G. Analysis of apoptotic and survival mediators in the early post-natal and mature retina. Exp. Eye Res. 2006, 83:1482-1492.
35. Ohh M., Kaelin W.G. The von Hippel-Lindau tumour suppressor protein: new perspectives. Mol. Med. Today 1999, 5:257-263.
36. Ohh M., Yauch R.L., Lonergan K.M., Whaley J.M., Stemmer-Rachamimov A.O., Louis D.N., Gavin B.J., Kley N., Kaelin W.G., Iliopoulos O. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol. Cell 1998, 1:959-968.
37. Peruzzi B., Athauda G., Bottaro D.P. The von Hippel-Lindau tumor suppressor gene product represses oncogenic beta-catenin signaling in renal carcinoma cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:14531-14536.
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. Schlichtenbrede F.C., MacNeil A., Bainbridge J.W., Tschernutter M., Thrasher A.J., Smith A.J., Ali R.R. Intraocular gene delivery of ciliary neurotrophic factor results in significant loss of retinal function in normal mice and in the Prph2Rd2/Rd2 model of retinal degeneration. Gene Ther. 2003, 10:523-527.
41. Schlisio S., Kenchappa R.S., Vredeveld L.C., George R.E., Stewart R., Greulich H., Shahriari K., Nguyen N.V., Pigny P., Dahia P.L., Pomeroy S.L., Maris J.M., Look A.T., Meyerson M., Peeper D.S., Carter B.D., Kaelin W.G. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev. 2008, 22:884-893.
42. Seeliger M.W., Grimm C., Stahlberg F., Friedburg C., Jaissle G., Zrenner E., Guo H., Reme C.E., Humphries P., Hofmann F., Biel M., Fariss R.N., Redmond T.M., Wenzel A. New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat. Genet. 2001, 29:70-74.
43. Seeliger M.W., Beck S.C., Pereyra-Munoz N., Dangel S., Tsai J.Y., Luhmann U.F., van de Pavert S.A., Wijnholds J., Samardzija M., Wenzel A., Zrenner E., Narfstrom K., Fahl E., Tanimoto N., Acar N., Tonagel F. In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy. Vis. Res. 2005, 45:3512-3519.
44. Senger D.R., Galli S.J., Dvorak A.M., Perruzzi C.A., Harvey V.S., Dvorak H.F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983, 219:983-985.
45. Tanimoto N., Muehlfriedel R.L., Fischer M.D., Fahl E., Humphries P., Biel M., Seeliger M.W. Vision tests in the mouse: functional phenotyping with electroretinography. Front. Biosci. 2009, 14:2730-2737.
46. Tennant D.A., Gottlieb E. HIF prolyl hydroxylase-3 mediates alpha-ketoglutarate-induced apoptosis and tumor suppression. J. Mol. Med. 2010, 88:839-849.
47. Tezel G. TNF-alpha signaling in glaucomatous neurodegeneration. Prog. Brain Res. 2008, 173:409-421.
48. Thiersch M., Lange C., Joly S., Heynen S., Le Y.Z., Samardzija M., Grimm C. Retinal neuroprotection by hypoxic preconditioning is independent of hypoxia-inducible factor-1 alpha expression in photoreceptors. Eur. J. Neurosci. 2009, 29:2291-2302.
49. 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.
50. van Rooijen E., Voest E.E., Logister I., Bussmann J., Korving J., van Eeden F.J., Giles R.H., Schulte-Merker S. von Hippel-Lindau tumor suppressor mutants faithfully model pathological hypoxia-driven angiogenesis and vascular retinopathies in zebrafish. Model Mech. 2010, 3:343-353.
51. Zeiss C.J., Neal J., Johnson E.A. Caspase-3 in postnatal retinal development and degeneration. Invest. Ophthalmol. Vis. Sci. 2004, 45:964-970.