The appropriateness of the mouse model for ataxia-telangiectasia: Neurological defects but no neurodegeneration

DNA Repair

Volumn 12, Issue 8, 2013, Pages 612-619

  Lavin, Martin F ^a,b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Ataxia telangiectasia; Atm; Mouse models; Neurodegeneration

Indexed keywords

ARTICLE; ATAXIA TELANGIECTASIA; CEREBELLUM ATROPHY; DISEASE MODEL; GRANULE CELL; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PURKINJE CELL;

ATAXIA-TELANGIECTASIA; ATM; MOUSE MODELS; NEURODEGENERATION;

ANIMALS; ATAXIA TELANGIECTASIA; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BRAIN; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; GENOMIC INSTABILITY; MICE; NEURODEGENERATIVE DISEASES; NEURONS; PHENOTYPE;

ATAXIA TELANGIECTASIA; MUS;

EID: 84880606646     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.04.014     Document Type: Article

References (83)

1. Boder E., Sedgwick R.P. Ataxia-telangiectasia, A familial syndrome of progressive cerebellar ataxia, oculocutaneous telangiectasia and frequent pulmonary infection. A preliminary report on 7 children, an autopsy, and a case history. Univ. South. Calif. Med. Bull. 1957, 9:15-28.
2. Gatti R.A., Berkel I., Boder E., Braedt G., Charmley P., et al. Localization of an ataxia-telangiectasia gene to chromosome 11q22-23. Nature 1988, 336:577-580.
3. Savitsky K., Bar-Shira A., Gilad S., Rotman G., Ziv Y., Vanagaite L., et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 1995, 268:1749-1753.
4. Sedgwick R.P., Boder E. Ataxia-telangiectasia. Handbook of Clinical Neurology, vol. 16. Hereditary Neuropathies and Spinocerebellar Atrophies 1991, 347-423. Elsevier, Amsterdam. J.M.B.V. De Jong (Ed.).
5. Boder E.E. Ataxia-telangiectasia: an overview. Kroc Found. Ser. 1985, 19:1-63.
6. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M.M., et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
7. Elson A., Wang Y., Daughertyl C.J., Morton C.C., Zhou F., et al. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. PNAS 1996, 93:13084-13089.
8. Xu Y., Baltimore D. Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 1996, 10:2401-2410.
9. Herzog K.H., Chong M.J., Kapsetaki M., Morgan J.I., McKinnon P.J. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 1998, 280:1089-1091.
10. Spring K., Cross S., Li C., Watters D., Ben-Senior L.L., et al. Atm knock-in mice harboring an in-frame detection corresponding to the human ATM 763del9 common mutation exhibit a variant phenotype. Cancer Res. 2001, 61:4561-4568.
11. Cappecchi M.R. The new mouse genetics: altering the genome by gene targeting. Trends Genet. 1989, 5:70-76.
12. Osborne L.R. Animal models of Williams syndrome. Am. J. Med. Genet. C Semin. Med. Genet. 2010, 154C:209-219.
13. Borghesani P.R., Alt F.W., Bottaro A., Davidson L., Aksov S., et al. Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:3336-3341.
14. Schubert R., Erker L., Barlow C., Yakushiji H., Larson D., et al. Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum. Mol. Genet. 2004, 13:1793-1802.
15. Manning T.S., Gibson G.R. Microbial-gut interactions in health and disease prebiotics. Best Pract. Res. Clin. Gastroenterol. 2004, 18:287-298.
16. Xu Y., Ashley T., Brainerd E.E., Bronson R.T., Meyn M.S., et al. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects and thymic lymphoma. Genes Dev. 1996, 10:2411-2422.
17. Kuljis R.O., Xu Y., Aguila M.C., Baltimore D. Degeneration of neurons, synpases, and neurophil and glial activation in a murine Atm knockout model of ataxia-telangiectasia. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:12688-12693.
18. Barlow C., Ribaut-Barassin C., Zwingman T.A., Pope A.J., Brown K.D., et al. ATM is a cytoplasmic protein in mouse brain required to prevent lysosomal accumulation. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:871-876.
19. Chen P., Peng C., Luff J., Spring K., Watters D., et al. Oxidative stress is responsible for deficient survival and dendritogenesis in purkinje neurons from ataxia-telangiectasia mutated mutant mice. J. Neurosci. 2003, 23:11453-11460.
20. Liu N., Stoica G., Yan M., Scofield V.L., Qiang W., Lynn W.S., Wong P.K. ATM deficiency induces oxidative stress and endoplasmic reticulum stress in astrocytes. Lab. Invest. 2005, 85:1471-1480.
21. Kim J.P.K. Oxidative stress is linked to ERK1/2 - p16 signalling mediated growth defect in ATM-deficient astrocytes. J. Biol. Chem. 2009, 284:14396-14404.
22. -/- mice is attributable to accumulation of reactive oxygen species. Biochem. Biophys. Res. Commun. 2012, 418:267-272.
23. Eliam R., Peter Y., Elson A., Rotman G., Shiloh Y., et al. Selective loss of dopaminergic nigro-striatal neurons in brains of Atm-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:12653-12656.
24. Fallon J.H., Moore R.Y. Catecholamine innervations of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 1978, 180:545-580.
25. Kirschner M., Galron R., Frenkel D., Mandelbaum G., Shiloh Y. Malfunctioning DNA damage response (DDR) leads to the degeneration of nigro-striatal pathway in mouse brain. J. Mol. Neurosci. 2012, 46:554-568.
26. Maser R.S., Monsen K.J., Nelms B.E., Petrini J.H. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double strand breaks. Mol. Cell. Biol. 1997, 17:6087-6096.
27. Uziel T., Lerenthal Y., Moyal L., Andegeko Y., Mittelman L., et al. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 2003, 22(2003):5612-5621.
28. Kozlov S.V., Graham M.E., Peng C., Chen P., Robinson P.J., et al. Involvement of novel autophosphorylation sites in ATM activation. EMBO J. 2006, 25:3504-3515.
29. Berkovich E., Monnat R.J., Kastan M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 2007, 9:683-690.
30. Lavin M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell Biol. 2008, 9:759-769.
31. Oba D., Havashi M., Minamitani M., Hamano S., Uchisaka N., Kikuchi A., Kishimoto H., Takagi M., Morio T., Mizutani S. Autopsy study of cerebellar degeneration in siblings with ataxia-telangiectasia-like disorder. Acta Neuropathol. 2010, 119:513-520.
32. Digweed M., Sperling K. Nijmegen breakage syndrome: clinical manifestation of defective response to DNA double-strand breaks. DNA Repair 2004, 3:1207-1217.
33. Dar I., Yosha G., Elfassy R., Galron R., Wang Z.Q., Shiloh Y., Barzilai A. Investigation of the functional link between ATM and NBS1 in the DNA damage response in the mouse cerebellum. J. Biol. Chem. 2011, 286:153561-153576.
34. Shull E.R., Lee Y., Nakane H., Stracker T.H., Zhao J., Russell H.R., Petrini J.H., McKinnon P.J. Differential DNA damage signalling accounts for distinct neural apoptotic responses in ATLD and NBS. Genes Dev. 2009, 171-180.
35. Browne S.E., Roberts L.J., Dennery P.A., Doctrow S.R., Beal M.F. Treatment with catalytic antioxidant corrects the neurobehavioral defect in ataxia-telangiectasia mice. Free Radic. Biol. Med. 2004, 36:938-942.
36. Raz-Prag D., Galron R., Segev-Amzaleg N., Solomon N., Shiloh A.S.Y., et al. A role for vascular deficiency in retinal pathology in a mouse model of ataxia-telangiectasia. Am. J. Pathol. 2011, 179:1533-1541.
37. Rotman G., Shiloh Y. Ataxia-telangiectasia: is ATM a sensor of oxidative damage and stress?. Bioessays 1997, 19:911-917.
38. Ziv S., Brenner O., Amariglio N., Smorodinsky N.I., Galron R., et al. Impaired genomic stability and increased oxidative stress exacerbate different features of ataxia-telangiectasia. Hum. Mol. Genet. 2005, 14:2929-2943.
39. Kamsler A., Daily D., Hochman A., Stern N., Shiloh Y., et al. Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res. 2001, 61:1849-1854.
40. Barbizhayev M.A. Mitochondria induce oxidative stress, generation of oxygen species and redox state unbalance of the eye lens leading to human cataract formation: disruption of redox lens organisation by phospholipid hydroperoxides as a common basis for cataract disease. Cell Biochem. Funct. 2011, 29:183-206.
41. McFarlin D.E., Strober W., Waldmann T.A. Ataxia-telangiectasia. Medicine (Baltimore) 1972, 51:281-314.
42. Thames H.D., Bentzen S.M., Turesson I., Overgaard M., Van den Bogaert W. Time-dose factors in radiotherapy: a review of the human data. Radiother. Oncol. 1990, 19:219-235.
43. Smith J.L., Cogan D.G. Ataxia-telangiectasia. Arch. Ophthalmol. 1959, 62:364-369.
44. Hyams S.W., Reisner S.H., Neumann E. The eye signs in ataxia-telangiectasia. Am. J. Ophthalmol. 1966, 62:1118-1124.
45. Antonetti D.A., Barber A.J., Khin S., Lieth E., Tarbell J.M., et al. Vascular permeability in experimental diabetes is associated with reduced endothelial occluding content: vascular endothelial growth factor decreases occluding in retinal endothelial cells. Penn State Retina Research Group. Diabetes 1998, 47:1953-1959.
46. Christoffel D.J., Golden S.A., Russo S.J. Structural and synaptic plasticity in stress-related disorders. Rev. Neurosci. 2011, 22:535-549.
47. Pagani E., Ginestroni A., Della R., Nave R., Agosta F., et al. Assessment of brain white matter fiber bundle atrophy in patients with Friedrich ataxia. Radiology 2010, 255:882-889.
48. Rutten W.L., Ruardij T.G., Marani E., Roelofsen B.H. Neural networks on chemically patterned electrode arrays: towards a cultured probe. Acta Neurochir. Suppl. 2007, 97:547-554.
49. Segev R., Benveniste M., Hulata E., Cohen N., Palevski A., et al. Long term behaviour of lithographically prepared in vitro neuronal networks. Phys. Rev. Lett. 2002, 88:1102-1181.
50. Levine-Small N., Yekutieli Z., Aljadeff J., Boccaletti S., Ben-Jacob E., et al. Reduced synchronization persistence in neural networks derived from Atm-deficient mice. Front Neurosci. 2011, 5:46.
51. Boehrs J.K., He J., Halaby M.J., Yang D.Q. Constitutive expression and cytoplasmic compartmentalisation of ATM protein in differentiated human neuron-like SH-SY5Y cells. J. Neurochem. 2007, 100:337-345.
52. Yang Y., Herrup K. Loss of neuronal cell cycle control in ataxia-telangiectasia: a unified disease mechanism. J. Neurosci. 2005, 25:2522-2529.
53. Kim T.S., Kawaguchi M., Suzuki M., Jung C.G., Asai K. (ATBF1) transcription factor induces PDGFRB which activates ATM in the cytoplasm to protect cerebellar neurons from oxidative stress. Dis. Model. Mech. 2010, 3:752-762.
54. Li J., Han Y.R., Plummer M.R., Herrup K. Cytoplasmic ATM in neurons modules synaptic function. Curr. Biol. 2009, 19:2091-2096.
55. O'Connor R.D., Linthicum D.S. Mitogen receptor redistribution defects and concomitant absence of blastogenesis in ataxia-telangiectasia T lymphocytes. Clin. Immunol. Immunopathol. 1980, 15:66-75.
56. Chiesa N., Barlow C., Wynshaw-Boris A., Strata P., et al. Atm-deficient mice Purkinje cells show age-dependent defects in calcium spike bursts and calcium currents. Neurosciece 2000, 96:575-583.
57. Bhatti S., Kozlov S., Farooqi A.A., Naqi A., Lavin M.F., et al. ATM protein kinase: the linchpin of cellular defences to stress. Cell. Mol. Life Sci. 2011, 68:2977-3006.
58. Biton S., Barzilai A., Shiloh Y.Y. The neurological phenotype of ataxia-tealngiectasia: solving a persistent puzzle. DNA Repair 2008, 7:1028-1038.
59. Barlow C., Dennery P.A., Shigenaga M.K., Smith M.A., et al. Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs. PNAS 1999, 96:9915-9919.
60. Alexander A., Cai S.L., Kim J., Nanez A., Sahin M., et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4153-4158.
61. Guo Z., Kozlov S., Lavin M.F., Person M.D., Paull T.T. ATM activation by oxidative stress. Science 2010, 330:517-521.
62. Shafman T., Khanna K.K., Kedar P., Spring K., Kozlov S.S., et al. Interaction between ATM protein and c-Abl in response to DNA damage. Nature 1997, 387:520-523.
63. Gatei M., Shkedy D., Khanna K.K., Uziel T., Shiloh Y., et al. Ataxia-telangiectasia: chronic activation of damage-responsive functions is reduced by alpha-lipoic acid. Oncogene 2001, 20:289-294.
64. Weizman N., Shiloh Y., Barzilai A.A. Contribution of the Atm protein to maintaining cellular homeostasis evidenced by continuous activation of the AP-1 pathway in Atm-deficient brains. J. Biol. Chem. 2003, 278:6741-6747.
65. Ambrose M., Goldstine J.V., Gatti R.A. Intrinsic mitochondrial dysfunction in ATM-deficient lymphoblastoid cells. Hum. Mol. Genet. 2007, 16:2154-2164.
66. Eaton J.S., Lin Z.P., Sartorelli A.C., Bonawitz N.D., Shadel G.S. Ataxia-telangiectasia mutated kinase regulates ribonucleotide reductase and mitochondrial homeostasis. Clin. Invest. 2007, 117:2723-2734.
67. Valentin-Vega Y.A., Maclean K.H., Tait-Mulder J., Milasta S., Steeves M., et al. Mitochondrial dysfunction in ataxia-telangiectasia. Blood 2012, 119:1490-1500.
68. Fransen M., Nordgren M., Wang B., Apanasets O. Role of peroxisomes in ROS/RNA-metabolism: implications for human disease. Biochim. Biophys. Acta 2011, 1822:1363-1373.
69. Watters D. Localisation of a portion of extranuclear ATM to peroxisomes. J. Biol. Chem. 1999, 274:34277-34282.
70. Stern N., Hochman A., Zemach N., Weizman N., Hammel I.I., et al. Accumulation of DNA damage and reduced levels of nicotine adenine dinucleotide in the brains of Atm-deficient mice. J. Biol. Chem. 2002, 277:602-608.
71. Quick K.K., Dugan L.L. Superoxide stress identifies neurons at risk in a model of ataxia-telangiectasia. Ann. Neurol. 2001, 49:627-635.
72. Peter Y., Rotman G., Lotem J., Elson A., Shiloh Y., et al. Elevated Cu/Zn-SOD exacerbates radiation sensitivity and hematopoietic abnormalities of Atm-deficient mice. EMBO J. 2001, 20:1538-1546.
73. Takao N., Yamamoto K. Protective roles for ATM in cellular response to oxidative stress. FEBS Lett. 2000, 472:133-136.
74. Berni A., Meschini R., Filippi S., Palitti F., De Amicis A.A., et al. l-Carnitine enhances resistance to oxidative stress by reducing DNA damage in ataxia telangiectasia cells. Mutat. Res. 2008, 650:165-174.
75. Pollard J.M., Reboucas J.S., Durazo A., Kos I., Fike F.F., et al. Radioprotective effects of manganese-containing superoxide dismutase mimics on ataxia telangiectasia cells. Free Radic. Biol. Med. 2009, 47:250-260.
76. Reliene R., Shiestl R.H. Antioxidant N-acetyl cysteine reduces incidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair 2006, 5:852-859.
77. Yan M., Qiang W., Liu N., Shen J., Lynn W.S., et al. The ataxia-telangiectasia gene product may modulate DNA turnover and control cell fate by regulating cellular redox in lymphocytes. FASEB J. 2001, 15:1132-1138.
78. -/- mice by dexamethasone. Cancer Res. 2002, 62:5153-5157.
79. Reliene R., Fischer E., Schiestl R.H. Effect of N-acetyl cysteine on oxidative DNA damage and the frequency of DNA deletions in Atm-deficient mice. Cancer Res. 2004, 64:5148-5153.
80. Gueven N., Luff J., Peng C., Hosokawa K., Bottle S.E., Lavin M.F. Dramatic extension of tumour latency and correction of neuro-behavioural phenotype in Atm-mutant mice with a nitroxide antioxidant. Free Radic. Biol. Med. 2006, 41:992-1000.
81. Nayler S., Gatei M., Kozlov S., Gatti R., Mar J.C., et al. Induced pluripotent stem cells from ataxia-telangiectasia recapitulate the cellular phenotype. Stem Cells Trans. Med. 2012, 1:523-535.
82. Li J., Chen J., Ricupero C.L., Hart R.P., Schwartz M.S., Kusnecov A., Herrup K. Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia. Nat. Med. 2012, 18:783-790.
83. Miles P.D., Treuner K., Latronica M., Olefsky J.M., Barlow C. Impaired insulin secretion in a mouse model of ataxia telangiectasia. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E70-E74.