"Super p53" Mice Display Retinal Astroglial Changes

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Salazar, Juan J ^a   Gallego Pinazo, Roberto ^c,d   de Hoz, Rosa ^a   Pinazo Durán, Maria D ^d   Rojas, Blanca ^a   Ramírez, Ana I ^a   Serrano, Manuel ^b   Ramírez, José M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b Structural Biology and Biocomputing Programme   (Spain)

^c HOSPITAL UNIVERSITARIO LA FE   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE STRUCTURE; IMMUNOHISTOCHEMISTRY; MACROGLIA; MOUSE; NONHUMAN; OXIDATIVE STRESS; P53 GENE; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RETINA CELL; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; ASTROCYTES; FLUORESCENT ANTIBODY TECHNIQUE; GLIAL FIBRILLARY ACIDIC PROTEIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RETINA; STAINING AND LABELING; TUMOR SUPPRESSOR PROTEIN P53;

MUS;

EID: 84878753289     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065446     Document Type: Article

References (84)

1. Ljungman M, (2000) Dial 9-1-1 for p53: Mechanisms of p53 activation by cellular stress. Neoplasia 2: 208-225.
2. Pluquet O, Hainaut P, (2001) Genotoxic and non-genotoxic pathways of p53 induction. Cancer Lett 174: 1-15.
3. Llanos S, Efeyan A, Monsech J, Dominguez O, Serrano M, (2006) A high-throughput loss-of-function screening identifies novel p53 regulators. Cell Cycle 5: 1880-1885.
4. Vousden KH, Lane DP, (2007) p53 in health and disease. Nat Rev Mol Cell Bio 8: 275-283.
5. Levine AJ, Oren M, (2009) The first 30 years of p53: Growing ever more complex. Nat Rev Cancer 9: 749-758.
6. Villasante A, Piazzolla D, Li H, Gómez-López G, Djabali M, et al. (2011) Epigenetic regulation of nanog expression by Ezh2 in pluripotent stem cells. Cell Cycle 10: 1488-1498.
7. Collado M, Serrano M, (2005) The senescent side of tumor suppression. Cell Cycle 4: 1722-1724.
8. Riley T, Sontag E, Chen P, Levine A, (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Bio 9: 402-412.
9. Suzuki K, Matsubara H (2011) Recent advances in p53 research and cancer treatment. J Biomed Biotechnol 2011: ID 978312.
10. Jebelli JD, Hooper C, Garden GA, Pocock JM, (2012) Emerging roles of p53 in glial cell function in health and disease. Glia 60: 515-525.
11. Cox LS, Lane DP, (1995) Tumour suppressors, kinases and clamps: How p53 regulates the cell cycle in response to DNA damage. Bioessays 17: 501-508.
12. Kippin TE, Martens DJ, Van Der Kooy D, (2005) p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Gene Dev 19: 756-767.
13. Meletis K, Wirta V, Hede SM, Nistér M, Lundeberg J, et al. (2006) p53 suppresses the self-renewal of adult neural stem cells. Development 133: 363-369.
14. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, et al. (2008) p53 and pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455: 1129-1133.
15. Villapol S, Acarin L, Faiz M, Castellano B, Gonzalez B, (2007) Distinct spatial and temporal activation of caspase pathways in neurons and glial cells after excitotoxic damage to the immature rat brain. J Neurosci Res 85: 3545-3556.
16. Yung HW, Bal-Price AK, Brown GC, Tolkovsky AM, (2004) Nitric oxide-induced cell death of cerebrocortical murine astrocytes is mediated through p53-and Bax-dependent pathways. J Neurochem 89: 812-821.
17. Bonini P, Cicconi S, Cardinale A, Vitale C, Serafino AL, et al. (2003) Oxidative stress induces p53-mediated apoptosis in glia: P53 transcription-independent way to die. J Neurosci Res 75: 83-95.
18. Matheu A, Maraver A, Klatt P, Flores I, Garcia-Cao I, et al. (2007) Delayed ageing through damage protection by the Arf/p53 pathway. Nature 448: 375-379.
19. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, et al. (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126: 107-120.
20. Joo CK, Choi JS, Ko HW, Park K, Sohn S, et al. (1999) Necrosis and apoptosis after retinal ischemia: Involvement of NMDA-mediated excitotoxicity and p53. Invest Ophthalmol Vis Sci 40: 713-720.
21. Morgan SE, Kastan MB, (1997) Foundations in cancer research p53 and ATM: Cell cycle, cell death, and cancer. Adv Cancer Res 71: 1-25.
22. Borges H, Chao C, Xu Y, Linden R, Wang J, (2004) Radiation-induced apoptosis in developing mouse retina exhibits dose-dependent requirement for ATM phosphorylation of p53. Cell Death Differ 11: 494-502.
23. Miller TJ, Schneider RJ, Miller JA, Martin BP, Al-Ubaidi MR, et al. (2006) Photoreceptor cell apoptosis induced by the 2-nitroimidazole radiosensitizer, CI-1010, is mediated by p53-linked activation of caspase-3. Neurotoxicology 27: 44-59.
24. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, et al. (2005) The antioxidant function of the p53 tumor suppressor. Nat Med 11: 1306-1313.
25. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, et al. (2006) P53 regulates mitochondrial respiration. Science 312: 1650-1653.
26. O'Connor JC, Wallace DM, O'Brien CJ, Cotter TG, (2008) A novel antioxidant function for the tumor-suppressor gene p53 in the retinal ganglion cell. Invest Ophthalmol Vis Sci 49: 4237-4244.
27. Wiegand R, Giusto NM, Rapp LM, Anderson RE, (1983) Evidence for rod outer segment lipid peroxidation following constant illumination of the rat retina. Invest Ophthalmol Vis Sci 24: 1433-1435.
28. Organisciak DT, Vaughan DK, (2010) Retinal light damage: Mechanisms and protection. Prog Ret Eye Res 29: 113-134.
29. Beatty S, Koh H, Phil M, Henson D, Boulton M, (2000) The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 45: 115.
30. Lipton SA, (2001) Retinal ganglion cells, glaucoma and neuroprotection. Prog Brain Res 131: 712-718.
31. Ohia SE, Opere CA, Leday AM, (2005) Pharmacological consequences of oxidative stress in ocular tissues. Mut Res 579: 22-36.
32. Zanon-Moreno V, Marco-Ventura P, Lleo-Perez A, Pons-Vazquez S, Garcia-Medina JJ, et al. (2008) Oxidative stress in primary open-angle glaucoma. J Glaucoma 17: 263-268.
33. Harada C, Namekata K, Guo X, Yoshida H, Mitamura Y, et al. (2010) ASK1 deficiency attenuates neural cell death in GLAST-deficient mice, a model of normal tension glaucoma. Cell Death Differ 17: 1751-1759.
34. Mancino R, Di Pierro D, Varesi C, Cerulli A, Feraco A, et al. (2011) Lipid peroxidation and total antioxidant capacity in vitreous, aqueous humor, and blood samples from patients with diabetic retinopathy. Mol Vis 17: 1298.
35. Hirrlinger PG, Ulbricht E, Iandiev I, Reichenbach A, Pannicke T, (2010) Alterations in protein expression and membrane properties during muller cell gliosis in a murine model of transient retinal ischemia. Neurosci Lett 472: 73-78.
36. Dirnagl U, Priller J, Dirnagl U, Priller J (2004) Focal cerebral ischemia: The multifaceted role of glial cells. Neuroglia. New York: Oxford.p 520.
37. Garcia-Cao I, Garcia-Cao M, Martin-Caballero J, Criado LM, Klatt P, et al. (2002) "Super p53" mice exhibit enhanced DNA damage response, are tumor resistant and age normally. EMBO J 21: 6225-6235.
38. Ramírez JM, Triviño A, Ramírez AI, Salazar JJ, García-Sánchez J, (1994) Immunohistochemical study of human retinal astroglia. Vision Res 34: 1935-1946.
39. Triviño A, Ramírez JM, Ramírez AI, Salazar JJ, García-Sánchez J, (1992) Retinal perivascular astroglia: An immunoperoxidase study. Vision Res 32: 1601-1607.
40. Ramírez AI, Salazar JJ, de Hoz R, Rojas B, Ruiz E, et al. (2006) Macroglial and retinal changes in hypercholesterolemic rabbits after normalization of cholesterol levels. Exp Eye Res 83: 1423-1438.
41. Ramírez AI, Salazar JJ, de Hoz R, Rojas B, Gallego BI, et al. (2010) Quantification of the effect of different levels of IOP in the astroglia of the rat retina ipsilateral and contralateral to experimental glaucoma. Invest Ophthalmol Vis Sci 51: 5690-5696.
42. Gallego BI, Salazar JJ, de Hoz R, Rojas B, Ramírez AI, et al. (2012) IOP induces upregulation of GFAP and MHC-II and microglia reactivity in mice retina contralateral to experimental glaucoma. J Neuroinflamm 9: 92.
43. Djebaïli M, Rondouin G, Baille V, Bockaert J, (2000) p53 and bax implication in NMDA induced-apoptosis in mouse hippocampus. Neuroreport 11: 2973-2976.
44. Martin LJ, Liu Z, (2002) Injury-induced spinal motor neuron apoptosis is preceded by DNA single-strand breaks and is p53-and Bax-dependent. J Neurobiol 50: 181-197.
45. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA, et al. (1996) Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 16: 1337-1345.
46. Napieralski JA, Raghupathi R, McIntosh TK, (1999) The tumor-suppressor gene, p53, is induced in injured brain regions following experimental traumatic brain injury. Mol Brain Res 71: 78-86.
47. Qin ZH, Chen RW, Wang Y, Nakai M, Chuang DM, et al. (1999) Nuclear factor κB nuclear translocation upregulates c-myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J Neurosci 19: 4023-4033.
48. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, et al. (1994) p53 induction is associated with neuronal damage in the central nervous system. PNAS 91: 7525-7529.
49. Watanabe H, Ohta S, Kumon Y, Sakaki S, Sakanaka M, (1999) Increase in p53 protein expression following cortical infarction in the spontaneously hypertensive rat. Brain Res 837: 38-45.
50. Malhotra S, Shnitka T, Elbrink J, (1990) Reactive astrocytes-a review. Cytobios 61: 133.
51. Ridet J, Privat A, (2000) Reactive astrocytes, their roles in CNS injury, and repair mechanisms. Adv Struct Biol 6: 147-185.
52. Pekny M, Nilsson M, (2005) Astrocyte activation and reactive gliosis. Glia 50: 427-434.
53. Malhotra A, Minja FJ, Crum A, Burrowes D, (2011) Ocular anatomy and cross-sectional imaging of the eye. Semin Ultrasound CT 32: 2-13.
54. Sofroniew M, Vinters H, (2010) Astrocytes: Biology and pathology. Acta Neuropathol 119: 7-35.
55. Allaman I, Bélanger M, Magistretti PJ, (2011) Astrocyte-neuron metabolic relationships: For better and for worse. Trends Neurosci 34: 76-87.
56. Tacconi MT, (1998) Neuronal death: Is there a role for astrocytes? Neurochem Res 23: 759-765.
57. Carson MJ, Cameron Thrash J, Walter B, (2006) The cellular response in neuroinflammation: The role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin Neurosci Res 6: 237-245.
58. Ueki Y, Karl MO, Sudar S, Pollak J, Taylor RJ, et al. (2012) P53 is required for the developmental restriction in müller glial proliferation in mouse retina. Glia 60: 1579-1589.
59. Tyner SD, Venkatachalam S, Choi J, Jones S, Ghebranious N, et al. (2002) p53 mutant mice that display early ageing-associated phenotypes. Nature 415: 45-53.
60. Madigan MC, Penfold PL, Provis JM, Balind TK, Billson FA, (1994) Intermediate filament expression in human retinal macroglia. histopathologic changes associated with age-related macular degeneration. Retina 14: 65-74.
61. Ramírez JM, Ramírez AI, Salazar JJ, de Hoz R, Triviño A, (2001) Changes of astrocytes in retinal ageing and age-related macular degeneration. Exp Eye Res 73: 601-615.
62. Cavallotti C, Cavallotti D, Pescosolido N, Pacella E, (2003) Age-related changes in rat optic nerve: Morphological studies. Anat Histol Embryol 32: 12-16.
63. Mansour H, Chamberlain CG, Weible MW 2nd, Hughes S, Chu Y, et al (2008) Aging-related changes in astrocytes in the rat retina: Imbalance between cell proliferation and cell death reduces astrocyte availability. Aging Cell 7: 526-540.
64. Ikui H, Uga S, Kohno T, (1976) Electron microscope study on astrocytes in the human retina using ruthenium red. Ophthalmic Res 8: 100-110.
65. Ramírez JM, Triviño A, Ramírez AI, Salazar JJ, García-Sánchez J, (1996) Structural specializations of human retinal glial cells. Vision Res 36: 2029-2036.
66. Zahs KR, Newman EA, (1997) Asymmetric gap junctional coupling between glial cells in the rat retina. Glia 20: 10-22.
67. Bussow H, (1980) The astrocytes in the retina and optic nerve head of mammals: A special glia for the ganglion cell axons. Cell Tissue Res 206: 367-378.
68. Hollander H, Makarov F, Dreher Z, van Driel D, Chan-Ling TL, et al. (1991) Structure of the macroglia of the retina: Sharing and division of labour between astrocytes and muller cells. J Comp Neurol 313: 587-603.
69. Ramson BR, Ye Z (2005) Gap junctions and hemichannels. In: Ketteman H, Ramson BR, editors. Neuroglia. Ney York: Oxford University Press. 177-189.
70. Gerdes HH, Bukoreshtliev NV, Barroso JFV, (2007) Tunneling nanotubes: A new route for the exchange of components between animal cells. FEBS Lett 581: 2194-2201.
71. Davis DM, Sowinski S, (2008) Membrane nanotubes: Dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 9: 431-436.
72. Zhang Y, (2011) Tunneling-nanotube: A new way of cell-cell communication. CIB 4: 324-325.
73. Wang M, Ma W, Zhao L, Fariss RN, Wong WT, (2011) Adaptive muller cell responses to microglial activation mediate neuroprotection and coordinate inflammation in the retina. J Neuroinflamm 8: 173.
74. Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, et al. (2009) M-sec promotes membrane nanotube formation by interacting with ral and the exocyst complex. Nat Cell Biol 11: 1427-1432.
75. Bensaad K, Vousden KH, (2005) Savior and slayer: The two faces of p53. Nat Med 11: 1278-1279.
76. Johnson TM, Yu ZX, Ferrans VJ, Lowenstein RA, Finkel T, (1996) Reactive oxygen species are downstream mediators of p53-dependent apoptosis. PNAS 93: 11848-11852.
77. Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B, (1997) A model for p53-induced apoptosis. Nature 389: 300-304.
78. Velasco-Miguel S, Buckbinder L, Jean P, Gelbert L, Talbott R, et al. (1999) PA26, a novel target of the p53 tumor suppressor and member of the GADD family of DNA damage and growth arrest inducible genes. Oncogene 18: 127.
79. Budanov AV, Sablina AA, Feinstein E, Koonin EV, Chumakov PM, (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Sci Signal 304: 596.
80. Yoon KA, Nakamura Y, Arakawa H, (2004) Identification of ALDH4 as a p53-inducible gene and its protective role in cellular stresses. J Hum Genet 49: 134-140.
81. Gu S, Liu Z, Pan S, Jiang Z, Lu H, et al. (2004) Global investigation of p53-induced apoptosis through quantitative proteomic profiling using comparative amino acid-coded tagging. Mol Cell Proteomics 3: 998-1008.
82. Wasylyk C, Wasylyk B, (2000) Defect in the p53-Mdm2 autoregulatory loop resulting from inactivation of TAFII250 in cell cycle mutant tsBN462 cells. Mol Cell Biol 20: 5554-5570.
83. Gallego-Pinazo R, Zanón-Moreno V, Sanz S, Andrés V, Serrano M, et al. (2008) Caracterización bioquímica del nervio óptico en el ratón que sobreexpresa el gen p53: Análisis de estrés oxidativo. Arch Soc Esp Oftalmol 83: 105-112.
84. Pinazo-Duran MD, Gallego-Pinazo R, Vinuesa Silva I, Zanon-Moreno V, Garcia-Medina JJ, et al. (2007) Biochemical determination of oxidative and antioxidant activities in the retina-choroid of the super P53 mice. ARVO Meeting Abstracts 48: 4180.