Retinal degeneration depends on Bmi1 function and reactivation of cell cycle proteins

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 7, 2013, Pages

  Zencak, Dusan ^a   Schouwey, Karine ^a   Chen, Danian ^b,e   Ekström, Per ^c   Tanger, Ellen ^d   Bremner, Rod ^b   Van Lohuizen, Maarten ^d   Arsenijevic, Yvan ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c LUND UNIVERSITY   (Sweden)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

^e SICHUAN UNIVERSITY   (China)

Author keywords

Blindness; Neurodegeneration; Polycomb

Indexed keywords

BMI1 PROTEIN; CELL CYCLE PROTEIN; TRANSCRIPTION FACTOR E2F1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA FRAGMENTATION; GENE LOCUS; MOUSE; NEUROPROTECTION; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA DEGENERATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VISUAL IMPAIRMENT;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CELL CYCLE PROTEINS; E2F1 TRANSCRIPTION FACTOR; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTOLOGICAL TECHNIQUES; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; POLYCOMB REPRESSIVE COMPLEX 1; PROTO-ONCOGENE PROTEINS; RETINAL DEGENERATION;

EID: 84873729483     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1108297110     Document Type: Article

References (50)

1. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368(9549):1795-1809. (Pubitemid 44739028)
2. LaVail MM, et al. (1998) Protection of mouse photoreceptors by survival factors in retinal degenerations. Invest Ophthalmol Vis Sci 39(3):592-602. (Pubitemid 28110693)
3. Frasson M, et al. (1999) Retinitis pigmentosa: Rod photoreceptor rescue by a calcium-channel blocker in the rd mouse. Nat Med 5(10):1183-1187. (Pubitemid 29474424)
4. Bennett J, et al. (1998) Adenovirus-mediated delivery of rhodopsin-promoted bcl-2 results in a delay in photoreceptor cell death in the rd/rd mouse. Gene Ther 5(9):1156-1164. (Pubitemid 28448422)
5. Paquet-Durand F, et al. (2011) A key role for cyclic nucleotide gated (CNG) channels in cGMP-related retinitis pigmentosa. Hum Mol Genet 20(5):941-947.
6. Vincent I, Rosado M, Davies P (1996) Mitotic mechanisms in Alzheimer's disease? J Cell Biol 132(3):413-425. (Pubitemid 26053445)
7. Yang Y, Geldmacher DS, Herrup K (2001) DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci 21(8):2661-2668. (Pubitemid 32298208)
8. Höglinger GU, et al. (2007) The pRb/E2F cell-cycle pathway mediates cell death in Parkinson's disease. Proc Natl Acad Sci USA 104(9):3585-3590. (Pubitemid 46364202)
9. Nguyen MD, et al. (2003) Cell cycle regulators in the neuronal death pathway of amyotrophic lateral sclerosis caused by mutant superoxide dismutase 1. J Neurosci 23(6):2131-2140. (Pubitemid 36368901)
10. Herrup K, Yang Y (2007) Cell cycle regulation in the postmitotic neuron: Oxymoron or new biology? Nat Rev Neurosci 8(5):368-378. (Pubitemid 46652467)
11. Appert-Collin A, et al. (2006) Cyclin dependent kinase inhibitors prevent apoptosis of postmitotic mouse motoneurons. Life Sci 79(5):484-490. (Pubitemid 43866127)
12. Park DS, Levine B, Ferrari G, Greene LA (1997) Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J Neurosci 17(23):8975-8983. (Pubitemid 27498426)
13. Osuga H, et al. (2000) Cyclin-dependent kinases as a therapeutic target for stroke. Proc Natl Acad Sci USA 97(18):10254-10259.
14. Menu dit Huart L, Lorentz O, Goureau O, Leveillard T, Sahel JA (2004) DNA repair in the degenerating mouse retina. Mol Cell Neurosci 26(3):441-449.
15. Chen D, et al. (2007) Rb-mediated neuronal differentiation through cell-cycle-independent regulation of E2f3a. PLoS Biol 5(7):e179.
16. Sharpless NE, DePinho RA (1999) The INK4A/ARF locus and its two gene products. Curr Opin Genet Dev 9(1):22-30. (Pubitemid 29080383)
17. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397(6715):164-168. (Pubitemid 29050921)
18. Wenzel A, Grimm C, Samardzija M, Remé CE (2005) Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res 24(2):275-306. (Pubitemid 40021788)
19. Lin SC, Skapek SX, Papermaster DS, Hankin M, Lee EY (2001) The proliferative and apoptotic activities of E2F1 in the mouse retina. Oncogene 20(48):7073-7084. (Pubitemid 33052199)
20. Wu L, et al. (2001) The E2F1-3 transcription factors are essential for cellular proliferation. Nature 414(6862):457-462. (Pubitemid 34173728)
21. Chen D, et al. (2009) Division and apoptosis of E2f-deficient retinal progenitors. Nature 462(7275):925-929.
22. Bruggeman SW, et al. (2005) Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev 19(12):1438-1443. (Pubitemid 41003010)
23. Boyer LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441(7091):349-353. (Pubitemid 44050199)
24. Kallin EM, et al. (2009) Genome-wide uH2A localization analysis highlights Bmi1-dependent deposition of the mark at repressed genes. PLoS Genet 5(6):e1000506.
25. Meng S, et al. (2010) Identification and characterization of Bmi-1-responding element within the human p16 promoter. J Biol Chem 285(43):33219-33229.
26. Tolhuis B, et al. (2006) Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38(6):694-699. (Pubitemid 43927313)
27. Seeliger MW, et al. (2001) New views on RPE65 deficiency: The rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat Genet 29(1):70-74. (Pubitemid 32801812)
28. Otani A, et al. (2002) Bone marrow-derived stem cells target retinal astrocytes and can promote or inhibit retinal angiogenesis. Nat Med 8(9):1004-1010. (Pubitemid 35033705)
29. Bennett J, et al. (1996) Photoreceptor cell rescue in retinal degeneration (rd) mice by in vivo gene therapy. Nat Med 2(6):649-654. (Pubitemid 26191951)
30. Punzo C, Kornacker K, Cepko CL (2009) Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci 12(1):44-52.
31. Léveillard T, et al. (2004) Identification and characterization of rod-derived cone viability factor. Nat Genet 36(7):755-759. (Pubitemid 38886639)
32. Takahashi M, Miyoshi H, Verma IM, Gage FH (1999) Rescue from photoreceptor degeneration in the rd mouse by human immunodeficiency virus vector-mediated gene transfer. J Virol 73(9):7812-7816. (Pubitemid 29383266)
33. Park DS, et al. (2000) Involvement of retinoblastoma family members and E2F/DP complexes in the death of neurons evoked by DNA damage. J Neurosci 20(9):3104-3114. (Pubitemid 30263127)
34. Wu J, Trogadis J, Bremner R (2001) Rod and cone degeneration in the rd mouse is p53 independent. Mol Vis 7:101-106. (Pubitemid 36153658)
35. Sherr CJ (2006) Divorcing ARF and p53: An unsettled case. Nat Rev Cancer 6(9):663-673.
36. Morris EJ, et al. (2001) Cyclin-dependent kinases and P53 pathways are activated independently and mediate Bax activation in neurons after DNA damage. J Neurosci 21(14):5017-5026. (Pubitemid 32622927)
37. Facchino S, Abdouh M, Chatoo W, Bernier G (2010) BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci 30(30):10096-10111.
38. Ismail IH, Andrin C, McDonald D, Hendzel MJ (2010) BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol 191(1):45-60.
39. Chatoo W, et al. (2009) The polycomb group gene Bmi1 regulates antioxidant defenses in neurons by repressing p53 pro-oxidant activity. J Neurosci 29(2):529-542.
40. Liu J, et al. (2009) Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459(7245):387-392.
41. Chen B, Cepko CL (2009) HDAC4 regulates neuronal survival in normal and diseased retinas. Science 323(5911):256-259.
42. Sancho-Pelluz J, et al. (2010) Excessive HDAC activation is critical for neurodegeneration in the rd1 mouse. Cell Death Dis 1:e24.
43. Bringmann A, et al. (2009) Cellular signaling and factors involved in Müller cell gliosis: Neuroprotective and detrimental effects. Prog Retin Eye Res 28(6):423-451.
44. Bruggeman SW, et al. (2007) Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell 12(4):328-341. (Pubitemid 47539307)
45. van der Lugt NM, et al. (1994) Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev 8(7):757-769.
46. Serrano M, et al. (1996) Role of the INK4a locus in tumor suppression and cell mortality. Cell 85(1):27-37. (Pubitemid 26116804)
47. Romijn HJ (1988) Development and advantages of serum-free, chemically defined nutrient media for culturing of nerve tissue. Biol Cell 63(3):263-268.
48. Romijn HJ, de Jong BM, Ruijter JM (1988) A procedure for culturing rat neocortex explants in a serum-free nutrient medium. J Neurosci Methods 23(1):75-83. (Pubitemid 18029119)
49. Caffé AR, et al. (2001) Mouse retina explants after long-term culture in serum free medium. J Chem Neuroanat 22(4):263-273. (Pubitemid 33082144)
50. Bemelmans AP, et al. (2006) Lentiviral gene transfer of RPE65 rescues survival and function of cones in a mouse model of Leber congenital amaurosis. PLoS Med 3(10):e347.