A role for vascular deficiency in retinal pathology in a mouse model of ataxia-telangiectasia

American Journal of Pathology

Volumn 179, Issue 3, 2011, Pages 1533-1541

  Raz Prag, Dorit ^a   Galron, Ronit ^a   Segev Amzaleg, Niva ^a   Solomon, Arieh S ^a   Shiloh, Yosef ^a   Barzilai, Ari ^a   Frenkel, Dan ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DNA; FIBRINOGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; OCCLUDIN; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ATAXIA TELANGIECTASIA; ATM PROTEIN DEFICIENCY; CONTROLLED STUDY; DNA DAMAGE; ELECTRORETINOGRAPHY; GENE MUTATION; GLIA CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RETINA DISEASE; TIGHT JUNCTION; WILD TYPE;

ANIMALS; ASTROCYTES; ATAXIA TELANGIECTASIA; ELECTRORETINOGRAPHY; ENDOTHELIUM, VASCULAR; MICE; RETINAL DISEASES; RETINAL HEMORRHAGE; TIGHT JUNCTIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80052847814     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.05.026     Document Type: Article

References (78)

1. H. Forstl, and R. Howard Recent studies on dementia senilis and brain disorders caused by atheromatous vascular disease: by A. Alzheimer, 1898 Alzheimer Dis Assoc Disord 5 1991 257 264
2. R.C. Baldwin, and J. O'Brien Vascular basis of late-onset depressive disorder Br J Psychiatry 180 2002 157 160 (Pubitemid 34142789)
3. B.V. Zlokovic The blood-brain barrier in health and chronic neurodegenerative disorders Neuron 57 2008 178 201
4. R.D. Bell, and B.V. Zlokovic Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease Acta Neuropath 118 2009 103 113
5. S.P. Jackson, and J. Bartek The DNA-damage response in human biology and disease Nature 461 2009 1071 1078
6. A. Ciccia, and S.J. Elledge The DNA damage response: making it safe to play with knives Mol Cell 40 2010 179 204
7. C.H. Bassing, and F.W. Alt The cellular response to general and programmed DNA double strand breaks DNA Repair (Amst) 3 2004 781 796 (Pubitemid 38997922)
8. A.J. Hartlerode, and R. Scully Mechanisms of double-strand break repair in somatic mammalian cells Biochem J 423 2009 157 168
9. M.F. Lavin, and S. Kozlov ATM activation and DNA damage response Cell Cycle 6 2007 931 942 (Pubitemid 46658748)
10. M.F. Lavin Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer Nat Rev Mol Cell Biol 9 2008 759 769
11. B. Halliwell Oxidative stress and neurodegeneration: where are we now? J Neurochem 97 2006 1634 1658 (Pubitemid 43873658)
12. J.J. Perry, L. Fan, and J.A. Tainer Developing master keys to brain pathology, cancer and aging from the structural biology of proteins controlling reactive oxygen species and DNA repair Neuroscience 145 2007 1280 1299 (Pubitemid 46656193)
13. S.W. Ryter, H.P. Kim, A. Hoetzel, J.W. Park, K. Nakahira, X. Wang, and A.M. Choi Mechanisms of cell death in oxidative stress Antioxid Redox Signal 9 2007 49 89 (Pubitemid 44901874)
14. E. Trushina, and C.T. McMurray Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases Neuroscience 145 2007 1233 1248 (Pubitemid 46602738)
15. C. Barlow, P.A. Dennery, M.K. Shigenaga, M.A. Smith, J.D. Morrow, L.J. Roberts 2nd, A. Wynshaw-Boris, and R.L. Levine Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs Proc Natl Acad Sci U S A 96 1999 9915 9919 (Pubitemid 29398832)
16. A. Barzilai, S. Biton, and Y. Shiloh The role of the DNA damage response in neuronal development, organization and maintenance DNA Repair (Amst) 7 2008 1010 1027
17. A. Barzilai, G. Rotman, and Y. Shiloh ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage DNA Repair (Amst) 1 2002 3 25 (Pubitemid 34475690)
18. P. Chen, C. Peng, J. Luff, K. Spring, D. Watters, S. Bottle, S. Furuya, and M.F. Lavin Oxidative stress is responsible for deficient survival and dendritogenesis in purkinje neurons from ataxia-telangiectasia mutated mutant mice J Neurosci 23 2003 11453 11460 (Pubitemid 37549702)
19. K. Ito, A. Hirao, F. Arai, S. Matsuoka, K. Takubo, I. Hamaguchi, K. Nomiyama, K. Hosokawa, K. Sakurada, N. Nakagata, Y. Ikeda, T.W. Mak, and T. Suda Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells Nature 431 2004 997 1002 (Pubitemid 39434422)
20. Z.E. Karanjawala, N. Murphy, D.R. Hinton, C.L. Hsieh, and M.R. Lieber Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants Curr Biol 12 2002 397 402 (Pubitemid 34209287)
21. A. Suraweera, O.J. Becherel, P. Chen, N. Rundle, R. Woods, J. Nakamura, M. Gatei, C. Criscuolo, A. Filla, L. Chessa, M. Fusser, B. Epe, N. Gueven, and M.F. Lavin Senataxin, defective in ataxia oculomotor apraxia type 2, is involved in the defense against oxidative DNA damage J Cell Biol 177 2007 969 979 (Pubitemid 46955702)
22. D.J. Watters Oxidative stress in ataxia telangiectasia Redox Rep 8 2003 23 29 (Pubitemid 36204249)
23. Z. Guo, S. Kozlov, M.F. Lavin, M.D. Person, and T.T. Paull ATM activation by oxidative stress Science 330 2010 517 521
24. T.O. Crawford, A.S. Mandir, M.A. Lefton-Greif, S.N. Goodman, B.K. Goodman, H. Sengul, and H.M. Lederman Quantitative neurologic assessment of ataxia-telangiectasia Neurology 54 2000 1505 1509 (Pubitemid 30210475)
25. M.F. Lavin, N. Gueven, S. Bottle, and R.A. Gatti Current and potential therapeutic strategies for the treatment of ataxia-telangiectasia Br Med Bull 81 2007
26. T.O. Crawford Ataxia telangiectasia Semin Pediatr Neurol 5 1998 287 294 (Pubitemid 29011304)
27. J. Leemput, C. Masson, K. Bigot, A. Errachid, A. Dansault, A. Provost, S. Gadin, S. Aoufouchi, M. Menasche, and M. Abitbol ATM localization and gene expression in the adult mouse eye Mol Vis 15 2009 393 416
28. C. Barlow, S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J.N. Crawley, T. Ried, D. Tagle, and A. Wynshaw-Boris Atm-deficient mice: a paradigm of ataxia telangiectasia Cell 86 1996 159 171 (Pubitemid 26259926)
29. D. Frenkel, L. Puckett, S. Petrovic, W. Xia, G. Chen, J. Vega, A. Dembinsky-Vaknin, J. Shen, M. Plante, D.S. Burt, and H.L. Weiner A nasal proteosome adjuvant activates microglia and prevents amyloid deposition Ann Neurol 63 2008 591 601
30. S. Biton, A. Barzilai, and Y. Shiloh The neurological phenotype of ataxia-telangiectasia: solving a persistent puzzle DNA Repair (Amst) 7 2008 1028 1038
31. M. Detmar, L.F. Brown, B. Berse, R.W. Jackman, B.M. Elicker, H.F. Dvorak, and K.P. Claffey Hypoxia regulates the expression of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) and its receptors in human skin J Invest Dermatol 108 1997 263 268 (Pubitemid 27116221)
32. D. Shweiki, A. Itin, D. Soffer, and E. Keshet Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis Nature 359 1992 843 845
33. N.S. Harhaj, and D.A. Antonetti Regulation of tight junctions and loss of barrier function in pathophysiology Int J Biochem Cell Biol 36 2004 1206 1237 (Pubitemid 38519069)
34. H.G. Blaauwgeers, G.M. Holtkamp, H. Rutten, A.N. Witmer, P. Koolwijk, T.A. Partanen, K. Alitalo, M.E. Kroon, A. Kijlstra, V.W. van Hinsbergh, and R.O. Schlingemann Polarized vascular endothelial growth factor secretion by human retinal pigment epithelium and localization of vascular endothelial growth factor receptors on the inner choriocapillaris Evidence for a trophic paracrine relation Am J Pathol 155 1999 421 428 (Pubitemid 29370392)
35. D.A. Antonetti, A.J. Barber, S. Khin, E. Lieth, J.M. Tarbell, and T.W. Gardner Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells Penn State Retina Research Group Diabetes 47 1998 1953 1959 (Pubitemid 28549205)
36. P. Hofman, H.G. Blaauwgeers, G.F. Vrensen, and R.O. Schlingemann Role of VEGF-A in endothelial phenotypic shift in human diabetic retinopathy and VEGF-A-induced retinopathy in monkeys Ophthalmic Res 33 2001 156 162 (Pubitemid 32424541)
37. N. Tyagi, A.M. Roberts, W.L. Dean, S.C. Tyagi, and D. Lominadze Fibrinogen induces endothelial cell permeability Mol Cell Biochem 307 2008 13 22 (Pubitemid 350238642)
38. A. Viswanathan, and H. Chabriat Cerebral microhemorrhage Stroke 37 2006 550 555 (Pubitemid 43732025)
39. V. Lifshitz, and D. Frenkel Animal models for cerebrovascular impairment and its relevance in vascular dementia M.L. Landow, Cognitive Impairment: Causes, Diagnosis and Treatments 2009 Nova Biomedical Books New York 1 20
40. M. Fruttiger Development of the retinal vasculature Angiogenesis 10 2007 77 88 (Pubitemid 46440628)
41. J. Kim, and P.K. Wong Oxidative stress is linked to ERK1/2-p16 signaling-mediated growth defect in ATM-deficient astrocytes J Biol Chem 284 2009 14396 14404
42. N. Otani, H. Nawashiro, S. Fukui, H. Ooigawa, A. Ohsumi, T. Toyooka, K. Shima, H. Gomi, and M. Brenner Enhanced hippocampal neurodegeneration after traumatic or kainate excitotoxicity in GFAP-null mice J Clin Neurosci 13 2006 934 938 (Pubitemid 44666419)
43. A.C. Pardo, V. Wong, L.M. Benson, M. Dykes, K. Tanaka, J.D. Rothstein, and N.J. Maragakis Loss of the astrocyte glutamate transporter GLT1 modifies disease in SOD1(G93A) mice Exp Neurol 201 2006 120 130 (Pubitemid 44223470)
44. N. Liu, G. Stoica, M. Yan, V.L. Scofield, W. Qiang, W.S. Lynn, and P.K. Wong ATM deficiency induces oxidative stress and endoplasmic reticulum stress in astrocytes Lab Invest 85 2005 1471 1480 (Pubitemid 41662332)
45. X.F. Wang, and M.S. Cynader Astrocytes provide cysteine to neurons by releasing glutathione J Neurochem 74 2000 1434 1442 (Pubitemid 30163963)
46. R.O. Kuljis, Y. Xu, M.C. Aguila, and D. Baltimore Degeneration of neurons, synapses, and neuropil and glial activation in a murine Atm knockout model of ataxia-telangiectasia Proc Natl Acad Sci U S A 94 1997 12688 12693 (Pubitemid 27492590)
47. E.C. Gosink, M.J. Chong, and P.J. McKinnon Ataxia telangiectasia mutated deficiency affects astrocyte growth but not radiosensitivity Cancer Res 59 1999 5294 5298 (Pubitemid 29503997)
48. D.Y. Yu, and S.J. Cringle Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease Prog Retin Eye Res 20 2001 175 208 (Pubitemid 32153715)
49. D.Y. Yu, and S.J. Cringle Retinal degeneration and local oxygen metabolism Exp Eye Res 80 2005 745 751 (Pubitemid 40798039)
50. C.E. Reme, U.F. Braschler, J. Roberts, and J. Dillon Light damage in the rat retina: effect of a radioprotective agent (WR-77913) on acute rod outer segment disk disruptions Photochem Photobiol 54 1991 137 142
51. S. Specht, M. Leffak, R.M. Darrow, and D.T. Organisciak Damage to rat retinal DNA induced in vivo by visible light Photochem Photobiol 69 1999 91 98 (Pubitemid 129555466)
52. I.A. Barbazetto, M. Room, N.A. Yannuzzi, G.R. Barile, J.E. Merriam, A.M. Bardal, K.B. Freund, L.A. Yannuzzi, and R. Allikmets ATM gene variants in patients with idiopathic perifoveal telangiectasia Invest Ophthalmol Vis Sci 49 2008 3806 3811
53. M. Mauget-Faysse, M. Vuillaume, M. Quaranta, N. Moullan, S. Angele, M.D. Friesen, and J. Hall Idiopathic and radiation-induced ocular telangiectasia: the involvement of the ATM gene Invest Ophthalmol Vis Sci 44 2003 3257 3262 (Pubitemid 36909756)
54. R.S. Kerbel Tumor angiogenesis N Engl J Med 358 2008 2039 2049 (Pubitemid 351656458)
55. P. Carmeliet Angiogenesis in health and disease Nat Med 9 2003 653 660 (Pubitemid 36749213)
56. L.P. Aiello, R.L. Avery, P.G. Arrigg, B.A. Keyt, H.D. Jampel, S.T. Shah, L.R. Pasquale, H. Thieme, M.A. Iwamoto, and J.E. Park Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders N Engl J Med 331 1994 1480 1487 (Pubitemid 24356306)
57. M.J. Tolentino, J.W. Miller, E.S. Gragoudas, F.A. Jakobiec, E. Flynn, K. Chatzistefanou, N. Ferrara, and A.P. Adamis Intravitreous injections of vascular endothelial growth factor produce retinal ischemia and microangiopathy in an adult primate Ophthalmology 103 1996 1820 1828 (Pubitemid 26403735)
58. P. Hofman, B.C. van Blijswijk, P.J. Gaillard, G.F. Vrensen, and R.O. Schlingemann Endothelial cell hypertrophy induced by vascular endothelial growth factor in the retina: new insights into the pathogenesis of capillary nonperfusion Arch Ophthalmol 119 2001 861 866 (Pubitemid 32530315)
59. S.E. D'Souza, V.J. Byers-Ward, E.E. Gardiner, H. Wang, and S.S. Sung Identification of an active sequence within the first immunoglobulin domain of intercellular cell adhesion molecule-1 (ICAM-1) that interacts with fibrinogen J Biol Chem 271 1996 24270 24277 (Pubitemid 26327416)
60. E.F. Plow, T.A. Haas, L. Zhang, J. Loftus, and J.W. Smith Ligand binding to integrins J Biol Chem 275 2000 21785 21788 (Pubitemid 30621742)
61. F.W. Luscinskas, and J. Lawler Integrins as dynamic regulators of vascular function FASEB J 8 1994 929 938 (Pubitemid 24286856)
62. W.D. Ehringer, S. Yamany, K. Steier, A. Farag, F.J. Roisen, A. Dozier, and F.N. Miller Quantitative image analysis of F-actin in endothelial cells Microcirculation 6 1999 291 303 (Pubitemid 129672569)
63. D. Lominadze, J.T. Saari, S.S. Percival, and D.A. Schuschke Proinflammatory effects of copper deficiency on neutrophils and lung endothelial cells Immunol Cell Biol 82 2004 231 238 (Pubitemid 38870015)
64. D. Mehta, and A.B. Malik Signaling mechanisms regulating endothelial permeability Physiol Rev 86 2006 279 367
65. R.L. Qiao, W. Yan, H. Lum, and A.B. Malik Arg-Gly-Asp peptide increases endothelial hydraulic conductivity: comparison with thrombin response Am J Physiol 269 1995 C110 C117
66. X. Trepat, M. Grabulosa, L. Buscemi, F. Rico, R. Farre, and D. Navajas Thrombin and histamine induce stiffening of alveolar epithelial cells J Appl Physiol 98 2005 1567 1574 (Pubitemid 40396539)
67. P.K. Patibandla, N. Tyagi, W.L. Dean, S.C. Tyagi, A.M. Roberts, and D. Lominadze Fibrinogen induces alterations of endothelial cell tight junction proteins J Cell Physiol 221 2009 195 203
68. M. Saitou, K. Fujimoto, Y. Doi, M. Itoh, T. Fujimoto, M. Furuse, H. Takano, T. Noda, and S. Tsukita Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions J Cell Biol 141 1998 397 408 (Pubitemid 28237088)
69. M. Saitou, M. Furuse, H. Sasaki, J.D. Schulzke, M. Fromm, H. Takano, T. Noda, and S. Tsukita Complex phenotype of mice lacking occludin, a component of tight junction strands Mol Biol Cell 11 2000 4131 4142
70. R.T. Abraham Cell cycle checkpoint signaling through the ATM and ATR kinases Genes Dev 15 2001 2177 2196 (Pubitemid 32843830)
71. R. Reliene, E. Fischer, and R.H. Schiestl Effect of N-acetyl cysteine on oxidative DNA damage and the frequency of DNA deletions in atm-deficient mice Cancer Res 64 2004 5148 5153 (Pubitemid 39006532)
72. D.M. Allen, H. van Praag, J. Ray, Z. Weaver, C.J. Winrow, T.A. Carter, R. Braquet, E. Harrington, T. Ried, K.D. Brown, F.H. Gage, and C. Barlow Ataxia telangiectasia mutated is essential during adult neurogenesis Genes Dev 15 2001 554 566 (Pubitemid 32205144)
73. P.R. Borghesani, F.W. Alt, A. Bottaro, L. Davidson, S. Aksoy, G.A. Rathbun, T.M. Roberts, W. Swat, R.A. Segal, and Y. Gu Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice Proc Natl Acad Sci U S A 97 2000 3336 3341 (Pubitemid 30183303)
74. N. Chiesa, C. Barlow, A. Wynshaw-Boris, P. Strata, and F. Tempia Atm-deficient mice Purkinje cells show age-dependent defects in calcium spike bursts and calcium currents Neuroscience 96 2000 575 583 (Pubitemid 30136322)
75. R. Eilam, Y. Peter, A. Elson, G. Rotman, Y. Shiloh, Y. Groner, and M. Segal Selective loss of dopaminergic nigro-striatal neurons in brains of Atm-deficient mice Proc Natl Acad Sci U S A 95 1998 12653 12656
76. R. Eilam, Y. Peter, Y. Groner, and M. Segal Late degeneration of nigro-striatal neurons in ATM-/- mice Neuroscience 121 2003 83 98 (Pubitemid 37297616)
77. H.T. Mount, J.C. Martel, P. Fluit, Y. Wu, E. Gallo-Hendrikx, C. Cosi, and M.R. Marien Progressive sensorimotor impairment is not associated with reduced dopamine and high energy phosphate donors in a model of ataxia-telangiectasia J Neurochem 88 2004 1449 1454 (Pubitemid 38366921)
78. M.D. Cabana, T.O. Crawford, J.A. Winkelstein, J.R. Christensen, and H.M. Lederman Consequences of the delayed diagnosis of ataxia-telangiectasia Pediatrics 102 1998 98 100 (Pubitemid 28309252)