Ras Homolog Enriched in the Brain is Linked to Retinal Ganglion Cell Apoptosis after Light Injury in Rats

Journal of Molecular Neuroscience

Volumn 54, Issue 2, 2014, Pages 243-251

  Shu, Qinmeng ^a   Xu, Yue ^b   Zhuang, Hong ^a   Fan, Jiawen ^a   Sun, Zhongcui ^a   Zhang, Meng ^a   Xu, Gezhi ^a  

^a FUDAN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Light induced retinal damage; Neuronal apoptosis; Rat; Retinal ganglion cells; Rheb

Indexed keywords

CASPASE 3; CDK4 PROTEIN, MOUSE; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROPEPTIDE; RHEB PROTEIN, MOUSE;

ADVERSE EFFECTS; ANIMAL; APOPTOSIS; GENETICS; LIGHT; MALE; METABOLISM; RADIATION RESPONSE; RAT; RETINA GANGLION CELL; RETINAL DEGENERATION; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; CASPASE 3; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; LIGHT; MALE; MONOMERIC GTP-BINDING PROTEINS; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RETINAL DEGENERATION; RETINAL GANGLION CELLS;

EID: 84896438034     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0281-z     Document Type: Article

References (47)

1. Arakawa-Takeuchi S, Kobayashi K, Park JH, Uranbileg B, Yamamoto H, Jinno S, Okayama H (2010) Mammalian target of rapamycin complex 1 signaling opposes the effects of anchorage loss, leading to activation of Cdk4 and Cdc6 stabilization. FEBS Lett 584:2779–2785
2. Arnault E, Barrau C, Nanteau C, Gondouin P, Bigot K, Vienot F, Gutman E, Fontaine V, Villette T, Cohen-Tannoudji D, Sahel JA, Picaud S (2013) Phototoxic action spectrum on a retinal pigment epithelium model of age-related macular degeneration exposed to sunlight normalized conditions. PLoS One 8:e71398
3. Augood CA, Vingerling JR, de Jong PT, Chakravarthy U, Seland J, Soubrane G, Tomazzoli L, Topouzis F, Bentham G, Rahu M, Vioque J, Young IS, Fletcher AE (2006) Prevalence of age-related maculopathy in older Europeans: the European Eye Study (EUREYE). Arch Ophthalmol 124:529–535
4. Becker EB, Bonni A (2004) Cell cycle regulation of neuronal apoptosis in development and disease. Prog Neurobiol 72:1–25
5. Cao M, Tan X, Jin W, Zheng H, Xu W, Rui Y, Li L, Cao J, Wu X, Cui G, Ke K, Gao Y (2013) Upregulation of Ras homolog enriched in the brain (Rheb) in lipopolysaccharide-induced neuroinflammation. Neurochem Int 62:406–417
6. Chahory S, Padron L, Courtois Y, Torriglia A (2004) The LEI/L-DNase II pathway is activated in light-induced retinal degeneration in rats. Neurosci Lett 367:205–209
7. Chen Z, Song Y, Yao J, Weng C, Yin ZQ (2013) Alterations of sodium and potassium channels of RGCs in RCS rat with the development of retinal degeneration. J Mol Neurosci 51(3):976–985
8. Dejda A, Jolivel V, Bourgault S, Seaborn T, Fournier A, Vaudry H, Vaudry D (2008) Inhibitory effect of PACAP on caspase activity in neuronal apoptosis: a better understanding towards therapeutic applications in neurodegenerative diseases. J Mol Neurosci 36:26–37
9. Donovan M, Carmody RJ, Cotter TG (2001) Light-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3-independent. J Biol Chem 276:23000–23008
10. Fletcher AE, Bentham GC, Agnew M, Young IS, Augood C, Chakravarthy U, de Jong PT, Rahu M, Seland J, Soubrane G, Tomazzoli L, Topouzis F, Vingerling JR, Vioque J (2008) Sunlight exposure, antioxidants, and age-related macular degeneration. Arch Ophthalmol 126:1396–1403
11. Friedman DS, O'Colmain BJ, Munoz B, Tomany SC, McCarty C, de Jong PT, Nemesure B, Mitchell P, Kempen J, Eye Diseases Prevalence Research G (2004) Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol 122:564–572
12. Garami A, Zwartkruis FJ, Nobukuni T, Joaquin M, Roccio M, Stocker H, Kozma SC, Hafen E, Bos JL, Thomas G (2003) Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol Cell 11:1457–1466
13. Garcia-Ayuso D, Salinas-Navarro M, Agudo-Barriuso M, Alarcon-Martinez L, Vidal-Sanz M, Villegas-Perez MP (2011) Retinal ganglion cell axonal compression by retinal vessels in light-induced retinal degeneration. Mol Vis 17:1716–1733
14. Harris TE, Lawrence JC Jr (2003) TOR signaling. Sci STKE 2003:re15
15. Hevroni D, Rattner A, Bundman M, Lederfein D, Gabarah A, Mangelus M, Silverman MA, Kedar H, Naor C, Kornuc M, Hanoch T, Seger R, Theill LE, Nedivi E, Richter-Levin G, Citri Y (1998) Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J Mol Neurosci 10:75–98
16. Hollyfield JG, Bonilha VL, Rayborn ME, Yang X, Shadrach KG, Lu L, Ufret RL, Salomon RG, Perez VL (2008) Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med 14:194–198
17. Karassek S, Berghaus C, Schwarten M, Goemans CG, Ohse N, Kock G, Jockers K, Neumann S, Gottfried S, Herrmann C, Heumann R, Stoll R (2010) Ras homolog enriched in brain (Rheb) enhances apoptotic signaling. J Biol Chem 285:33979–33991
18. Katai N, Yoshimura N (1999) Apoptotic retinal neuronal death by ischemia-reperfusion is executed by two distinct caspase family proteases. Invest Ophthalmol Vis Sci 40:2697–2705
19. Kermer P, Klocker N, Labes M, Thomsen S, Srinivasan A, Bahr M (1999) Activation of caspase-3 in axotomized rat retinal ganglion cells in vivo. FEBS Lett 453:361–364
20. Kruman II, Wersto RP, Cardozo-Pelaez F, Smilenov L, Chan SL, Chrest FJ, Emokpae R Jr, Gorospe M, Mattson MP (2004) Cell cycle activation linked to neuronal cell death initiated by DNA damage. Neuron 41:549–561
21. Lim LS, Mitchell P, Seddon JM, Holz FG, Wong TY (2012) Age-related macular degeneration. Lancet 379:1728–1738
22. Liu DX, Greene LA (2001) Neuronal apoptosis at the G1/S cell cycle checkpoint. Cell Tissue Res 305:217–228
23. Marc RE, Jones BW, Watt CB, Vazquez-Chona F, Vaughan DK, Organisciak DT (2008) Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis 14:782–806
24. Marco-Gomariz MA, Hurtado-Montalban N, Vidal-Sanz M, Lund RD, Villegas-Perez MP (2006) Phototoxic-induced photoreceptor degeneration causes retinal ganglion cell degeneration in pigmented rats. J Comp Neurol 498:163–179
25. Men J, Zhang X, Yang Y, Gao D (2012) An AD-related neuroprotector rescues transformed rat retinal ganglion cells from CoCl(2)-induced apoptosis. J Mol Neurosci 47:144–149
26. Nie D, Di Nardo A, Han JM, Baharanyi H, Kramvis I, Huynh T, Dabora S, Codeluppi S, Pandolfi PP, Pasquale EB, Sahin M (2010) Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat Neurosci 13:163–172
27. Organisciak DT, Vaughan DK (2010) Retinal light damage: mechanisms and protection. Prog Retin Eye Res 29:113–134
28. Osuga H, Osuga S, Wang F, Fetni R, Hogan MJ, Slack RS, Hakim AM, Ikeda JE, Park DS (2000) Cyclin-dependent kinases as a therapeutic target for stroke. Proc Natl Acad Sci U S A 97:10254–10259
29. Parrales A, López E, Lee-Rivera I, López-Colomé AM (2013) ERK1/2-dependent activation of mTOR/mTORC1/p70S6K regulates thrombin-induced RPE cell proliferation. Cell Signal 25(4):829–838
30. Peng Y, Zhang J, Xu H, He J, Ying X, Wang Y (2013) Neuroprotective effect of protease-activated receptor-2 in the hypoxia-induced apoptosis of rat RGC-5 cells. J Mol Neurosci 50:98–108
31. Randazzo J, Zhang Z, Hoff M, Kawada H, Sachs A, Yuan Y, Haider N, Kador P (2011) Orally active multi-functional antioxidants are neuroprotective in a rat model of light-induced retinal damage. PLoS One 6:e21926
32. Rein DB, Wittenborn JS, Zhang X, Honeycutt AA, Lesesne SB, Saaddine J, Vision Health Cost-Effectiveness Study, G (2009) Forecasting age-related macular degeneration through the year 2050: the potential impact of new treatments. Arch Ophthalmol 127:533–540
33. Ru W, Peng Y, Zhong L, Tang SJ (2012) A role of the mammalian target of rapamycin (mTOR) in glutamate-induced down-regulation of tuberous sclerosis complex proteins 2 (TSC2). J Mol Neurosci 47:340–345
34. Sabatini DM (2006) mTOR and cancer: insights into a complex relationship. Nat Rev Cancer 6:729–734
35. Saito K, Araki Y, Kontani K, Nishina H, Katada T (2005) Novel role of the small GTPase Rheb: its implication in endocytic pathway independent of the activation of mammalian target of rapamycin. J Biochem 137:423–430
36. Schwartz EI, Smilenov LB, Price MA, Osredkar T, Baker RA, Ghosh S, Shi FD, Vollmer TL, Lencinas A, Stearns DM, Gorospe M, Kruman II (2007) Cell cycle activation in postmitotic neurons is essential for DNA repair. Cell Cycle 6:318–329
37. Seddon JM, Reynolds R, Yu Y, Daly MJ, Rosner B (2011) Risk models for progression to advanced age-related macular degeneration using demographic, environmental, genetic, and ocular factors. Ophthalmology 118:2203–2211
38. Smith W, Assink J, Klein R, Mitchell P, Klaver CC, Klein BE, Hofman A, Jensen S, Wang JJ, de Jong PT (2001) Risk factors for age-related macular degeneration: pooled findings from three continents. Ophthalmology 108:697–704
39. Sparrow JR, Cai B (2001) Blue light-induced apoptosis of A2E-containing RPE: involvement of caspase-3 and protection by Bcl-2. Invest Ophthalmol Vis Sci 42(6):1356–1362
40. Springer JE, Nottingham SA, McEwen ML, Azbill RD, Jin Y (2001) Caspase-3 apoptotic signaling following injury to the central nervous system. Clin Chem Lab Med 39:299–307
41. Steindl-Kuscher K, Krugluger W, Boulton ME, Haas P, Schrattbauer K, Feichtinger H, Adlassnig W, Binder S (2009) Activation of the beta-catenin signaling pathway and its impact on RPE cell cycle. Invest Ophthalmol Vis Sci 50(9):4471–4476. doi:10.1167/iovs.08-3139
42. Wang T, Lao U, Edgar BA (2009) TOR-mediated autophagy regulates cell death in Drosophila neurodegenerative disease. J Cell Biol 186:703–711
43. Xu Y, Yang L, et al. Spatiotemporal Changes in NFATc4 expression of retinal ganglion cells after light-induced damage. J Mol Neurosci. (2013); doi 10.1007/s12031-013-0198-y
44. Yang Y, Mufson EJ, Herrup K (2003) Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J Neurosci 23:2557–2563
45. Young RW (1987) Pathophysiology of age-related macular degeneration. Surv Ophthalmol 31:291–306
46. Zhang M, Xu G, Liu W, Ni Y, Zhou W (2012) Role of fractalkine/CX3CR1 interaction in light-induced photoreceptor degeneration through regulating retinal microglial activation and migration. PLoS One 7:e35446
47. Zou J, Zhou L, Du XX, Ji Y, Xu J, Tian J, Jiang W, Zou Y, Yu S, Gan L, Luo M, Yang Q, Cui Y, Yang W, Xia X, Chen M, Zhao X, Shen Y, Chen PY, Worley PF, Xiao B (2011) Rheb1 is required for mTORC1 and myelination in postnatal brain development. Dev Cell 20:97–108