Reducing mitochondrial ROS improves disease-related pathology in a mouse model of ataxia-telangiectasia

Molecular Therapy

Volumn 21, Issue 1, 2013, Pages 42-48

  D'Souza, Anthony D ^a   Parish, Ian A ^a   Krause, Diane S ^a   Kaech, Susan M ^a,b   Shadel, Gerald S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; LACTIC ACID; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOCHONDRIAL CATALASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA TELANGIECTASIA; BONE MARROW; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; HEMATOPOIESIS; IN VITRO STUDY; MEMORY T LYMPHOCYTE; MITOCHONDRION; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ATAXIA TELANGIECTASIA; MUS;

EID: 84871927066     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.203     Document Type: Article

References (42)

1. Savitsky, K, Bar-Shira, A, Gilad, S, Rotman, G, Ziv, Y, Vanagaite, L et al. (1995). Asingle ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749-1753.
2. Barlow, C, Hirotsune, S, Paylor, R, Liyanage, M, Eckhaus, M, Collins, F et al. (1996).Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86: 159-171. (Pubitemid 26259926)
3. D'Souza, AD, Parish, IA, McKay, SE, Kaech, SM and Shadel, GS (2011). AberrantCD8+ T-cell responses and memory differentiation upon viral infection of an ataxiatelangiectasiamouse model driven by hyper-activated Akt and mTORC1 signaling.Am J Pathol 178: 2740-2751.
4. Ito, K, Hirao, A, Arai, F, Matsuoka, S, Takubo, K, Hamaguchi, I et al. (2004). Regulationof oxidative stress by ATM is required for self-renewal of haematopoietic stem cells.Nature 431: 997-1002. (Pubitemid 39434422)
5. Ito, K, Takubo, K, Arai, F, Satoh, H, Matsuoka, S, Ohmura, M et al. (2007). Regulationof reactive oxygen species by Atm is essential for proper response to DNA doublestrandbreaks in lymphocytes. J Immunol 178: 103-110. (Pubitemid 46039661)
6. Alexander, A, Cai, SL, Kim, J, Nanez, A, Sahin, M, MacLean, KH et al. (2012). ATMsignals to TSC2 in the cytoplasm to regulate TORC1 in response to ROS. Proc NatlAcad Sci USA 107: 4153-4158.
7. Kamsler, A, Daily, D, Hochman, A, Stern, N, Shiloh, Y, Rotman, G et al. (2001).Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redoxstate of brains from Atm-deficient mice. Cancer Res 61: 1849-1854. (Pubitemid 32691998)
8. Barlow, C, Dennery, PA, Shigenaga, MK, Smith, MA, Morrow, JD, Roberts, LJ 2nd et al.(1999). Loss of the ataxia-telangiectasia gene product causes oxidative damage intarget organs. Proc Natl Acad Sci USA 96: 9915-9919. (Pubitemid 29398832)
9. Reichenbach, J, Schubert, R, Schindler, D, Müller, K, Böhles, H and Zielen, S (2002).Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid Redox Signal4: 465-469. (Pubitemid 34753385)
10. Reliene, R and Schiestl, RH (2006). Antioxidant N-acetyl cysteine reducesincidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair (Amst)5: 852-859. (Pubitemid 43928890)
11. Schubert, R, Erker, L, Barlow, C, Yakushiji, H, Larson, D, Russo, A et al. (2004). Cancerchemoprevention by the antioxidant tempol in Atm-deficient mice. Hum Mol Genet13: 1793-1802. (Pubitemid 39173448)
12. Kuang, X, Shen, J, Wong, PK and Yan, M (2009). Deregulation of mTOR signalingis involved in thymic lymphoma development in Atm-/-mice. Biochem Biophys ResCommun 383: 368-372.
13. Eaton, JS, Lin, ZP, Sartorelli, AC, Bonawitz, ND and Shadel, GS (2007). Ataxiatelangiectasiamutated kinase regulates ribonucleotide reductase and mitochondrialhomeostasis. J Clin Invest 117: 2723-2734. (Pubitemid 47494372)
14. Ambrose, M, Goldstine, JV and Gatti, RA (2007). Intrinsic mitochondrial dysfunction inATM-deficient lymphoblastoid cells. Hum Mol Genet 16: 2154-2164. (Pubitemid 47354898)
15. Valentin-Vega, YA, Maclean, KH, Tait-Mulder, J, Milasta, S, Steeves, M, Dorsey, FC et al.(2012). Mitochondrial dysfunction in ataxia-telangiectasia. Blood 119: 1490-1500.
16. Shadel, GS (2008). Expression and maintenance of mitochondrial DNA: new insightsinto human disease pathology. Am J Pathol 172: 1445-1456.
17. Guo, Z, Kozlov, S, Lavin, MF, Person, MD and Paull, TT (2010). ATM activation byoxidative stress. Science 330: 517-521.
18. Ditch, S and Paull, TT (2012). The ATM protein kinase and cellular redox signaling:beyond the DNA damage response. Trends Biochem Sci 37: 15-22.
19. Schriner, SE, Linford, NJ, Martin, GM, Treuting, P, Ogburn, CE, Emond, M et al.(2005). Extension of murine life span by overexpression of catalase targeted tomitochondria. Science 308: 1909-1911. (Pubitemid 40941874)
20. Woo, DK, Green, PD, Santos, JH, D'Souza, AD, Walther, Z, Martin, WD et al. (2012).Mitochondrial genome instability and ROS enhance intestinal tumorigenesis inAPC(Min/+) mice. Am J Pathol 180: 24-31.
21. Goh, J, Enns, L, Fatemie, S, Hopkins, H, Morton, J, Pettan-Brewer, C et al. (2011).Mitochondrial targeted catalase suppresses invasive breast cancer in mice. BMC Cancer11: 191.
22. Treuting, PM, Linford, NJ, Knoblaugh, SE, Emond, MJ, Morton, JF, Martin, GM etal. (2008). Reduction of age-associated pathology in old mice by overexpression ofcatalase in mitochondria. J Gerontol A Biol Sci Med Sci 63: 813-822.
23. Someya, S, Xu, J, Kondo, K, Ding, D, Salvi, RJ, Yamasoba, T et al. (2009). Age-relatedhearing loss in C57BL/6J mice is mediated by Bak-dependent mitochondrial apoptosis.Proc Natl Acad Sci USA 106: 19432-19437.
24. Lee, HY, Choi, CS, Birkenfeld, AL, Alves, TC, Jornayvaz, FR, Jurczak, MJ et al. (2010).Targeted expression of catalase to mitochondria prevents age-associated reductions inmitochondrial function and insulin resistance. Cell Metab 12: 668-674.
25. Dai, DF, Johnson, SC, Villarin, JJ, Chin, MT, Nieves-Cintrón, M, Chen, T et al. (2011).Mitochondrial oxidative stress mediates angiotensin II-induced cardiac hypertrophyand Galphaq overexpression-induced heart failure. Circ Res 108: 837-846.
26. Xu, Y, Ashley, T, Brainerd, EE, Bronson, RT, Meyn, MS and Baltimore, D (1996).Targeted disruption of ATM leads to growth retardation, chromosomalfragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev10: 2411-2422. (Pubitemid 26341877)
27. Liyanage, M, Weaver, Z, Barlow, C, Coleman, A, Pankratz, DG, Anderson, S et al.(2000). Abnormal rearrangement within the alpha/delta T-cell receptor locus inlymphomas from Atm-deficient mice. Blood 96: 1940-1946. (Pubitemid 30661081)
28. Kuang, X, Yan, M, Liu, N, Scofield, VL, Qiang, W, Cahill, J et al. (2005). Control ofAtm-/-thymic lymphoma cell proliferation in vitro and in vivo by dexamethasone.Cancer Chemother Pharmacol 55: 203-212. (Pubitemid 40142884)
29. Kalyanaraman, B, Darley-Usmar, V, Davies, KJ, Dennery, PA, Forman, HJ, Grisham,MB et al. (2012). Measuring reactive oxygen and nitrogen species with fluorescentprobes: challenges and limitations. Free Radic Biol Med 52: 1-6.
30. Hishiya, A, Ito, M, Aburatani, H, Motoyama, N, Ikeda, K and Watanabe, K (2005).Ataxia telangiectasia mutated (Atm) knockout mice as a model of osteopenia due toimpaired bone formation. Bone 37: 497-503. (Pubitemid 41317323)
31. Yalcin, S, Zhang, X, Luciano, JP, Mungamuri, SK, Marinkovic, D, Vercherat, C et al.(2008). Foxo3 is essential for the regulation of ataxia telangiectasia mutated andoxidative stress-mediated homeostasis of hematopoietic stem cells. J Biol Chem283: 25692-25705.
32. Reliene, R and Schiestl, RH (2007). Antioxidants suppress lymphoma and increaselongevity in Atm-deficient mice. J Nutr 137 (suppl. 1): 229S-232S. (Pubitemid 46074948)
33. Browne, SE, Roberts, LJ 2nd, Dennery, PA, Doctrow, SR, Beal, MF, Barlow, C et al.(2004). Treatment with a catalytic antioxidant corrects the neurobehavioral defect inataxia-telangiectasia mice. Free Radic Biol Med 36: 938-942. (Pubitemid 38352909)
34. Chen, C, Liu, Y, Liu, R, Ikenoue, T, Guan, KL, Liu, Y et al. (2008). TSC-mTOR maintainsquiescence and function of hematopoietic stem cells by repressing mitochondrialbiogenesis and reactive oxygen species. J Exp Med 205: 2397-2408.
35. Armata, HL, Golebiowski, D, Jung, DY, Ko, HJ, Kim, JK and Sluss, HK (2010).Requirement of the ATM/p53 tumor suppressor pathway for glucose homeostasis. MolCell Biol 30: 5787-5794.
36. Sun, Y, Connors, KE and Yang, DQ (2007). AICAR induces phosphorylation ofAMPK in an ATM-dependent, LKB1-independent manner. Mol Cell Biochem 306:239-245. (Pubitemid 350001836)
37. Yan, M, Qiang, W, Liu, N, Shen, J, Lynn, WS and Wong, PK (2001). The ataxiatelangiectasiagene product may modulate DNA turnover and control cell fate byregulating cellular redox in lymphocytes. FASEB J 15: 1132-1138. (Pubitemid 32436298)
38. Kuang, X, Yan, M, Ajmo, JM, Scofield, VL, Stoica, G and Wong, PK (2012).Activation of AMP-activated protein kinase in cerebella of Atm-/-mice is attributableto accumulation of reactive oxygen species. Biochem Biophys Res Commun 418:267-272.
39. Peter, Y, Rotman, G, Lotem, J, Elson, A, Shiloh, Y and Groner, Y (2001). Elevated Cu/Zn-SOD exacerbates radiation sensitivity and hematopoietic abnormalities of Atmdeficientmice. EMBO J 20: 1538-1546. (Pubitemid 32299391)
40. Erker, L, Schubert, R, Elchuri, S, Huang, TT, Tarin, D, Mueller, K et al. (2006). Effect ofthe reduction of superoxide dismutase 1 and 2 or treatment with alpha-tocopherol ontumorigenesis in Atm-deficient mice. Free Radic Biol Med 41: 590-600. (Pubitemid 44080511)
41. West, AP, Brodsky, IE, Rahner, C, Woo, DK, Erdjument-Bromage, H, Tempst, Pet al. (2011). TLR signalling augments macrophage bactericidal activity throughmitochondrial ROS. Nature 472: 476-480.
42. Kaech, SM, Tan, JT, Wherry, EJ, Konieczny, BT, Surh, CD and Ahmed, R (2003).Selective expression of the interleukin 7 receptor identifies effector CD8 T cells thatgive rise to long-lived memory cells. Nat Immunol 4: 1191-1198. (Pubitemid 37540688)