Oxidative stress, mitochondrial abnormalities and antioxidant defense in Ataxia-telangiectasia, Bloom syndrome and Nijmegen breakage syndrome

Redox Biology

Volumn 11, Issue , 2017, Pages 375-383

  Maciejczyk, Mateusz ^a   Mikoluc, Bozena ^a   Pietrucha, Barbara ^b   Heropolitanska Pliszka, Edyta ^b   Pac, Malgorzata ^b   Motkowski, Radosław ^a   Car, Halina ^a  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

^b CHILDREN'S MEMORIAL HEALTH INSTITUTE   (Poland)

Author keywords

Antioxidants; Ataxia telangiectasia (A T); Bloom syndrome (BS); Nijmegen breakage syndrome (NBS); Oxidative damage; Oxidative stress

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; ANTIOXIDANT; ATM PROTEIN; CARNITINE; DEXAMETHASONE; EUK 189; FULVENE 5; IRON; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OXIDIZED LOW DENSITY LIPOPROTEIN; PYRROLIDINE DITHIOCARBAMATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RETINOL; TEMPOL; UNCLASSIFIED DRUG; LOW DENSITY LIPOPROTEIN; NOX4 PROTEIN, HUMAN;

ANTIOXIDANT ACTIVITY; ATAXIA TELANGIECTASIA; BLOOM SYNDROME; CELL DAMAGE; CELL PROTECTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DNA REPAIR; DRUG TARGETING; HUMAN; LIPID PEROXIDATION; LYMPHOMA; MITOCHONDRIAL RESPIRATION; MITOPHAGY; NIJMEGEN BREAKAGE SYNDROME; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; PATHOLOGY; SIGNAL TRANSDUCTION;

ATAXIA TELANGIECTASIA; BLOOM SYNDROME; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; HUMANS; LIPOPROTEINS, LDL; MITOCHONDRIA; NADPH OXIDASE 4; NIJMEGEN BREAKAGE SYNDROME; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 85007524587     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2016.12.030     Document Type: Review

References (71)

1. [1] Squadrone, S., Brizio, P., Mancini, C., Pozzi, E., Cavalieri, S., Abete, M.C., Brusco, A., Blood metal levels and related antioxidant enzyme activities in patients with ataxia telangiectasia. Neurobiol. Dis. 81 (2015), 162–167, 10.1016/j.nbd.2015.04.001.
2. [2] Perrone, S., Lotti, F., Geronzi, U., Guidoni, E., Longini, M., Buonocore, G., Oxidative stress in cancer-prone genetic diseases in pediatric age: the role of mitochondrial dysfunction. Oxid. Med. Cell. Longev. 2016 (2016), 1–7, 10.1155/2016/4782426.
3. [3] Taylor, A.M.R., Chromosome instability syndromes. Best. Pract. Res. Clin. Haematol. 14 (2001), 631–644, 10.1053/beha.2001.0158.
4. [4] Barzilai, A., Rotman, G., Shiloh, Y., ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage. DNA Repair 1 (2002), 3–25, 10.1016/S1568-7864(01)00007-6.
5. [5] Chun, H.H., Gatti, R.A., Ataxia-telangiectasia, an evolving phenotype. DNA Repair (Amst.). 3 (2004), 1187–1196, 10.1016/j.dnarep.2004.04.010.
6. [6] Ambrose, M., Goldstine, J.V., Gatti, R.A., Intrinsic mitochondrial dysfunction in ATM-deficient lymphoblastoid cells. Hum. Mol. Genet. 16 (2007), 2154–2164, 10.1093/hmg/ddm166.
7. [7] Taylor, A., Shang, F., Nowell, T., Galanty, Y., Shiloh, Y., Ubiquitination capabilities in response to neocarzinostatin and H(2)O(2) stress in cell lines from patients with ataxia-telangiectasia. Oncogene 21 (2002), 4363–4373, 10.1038/sj.onc.1205557.
8. [8] Shiloh, Y., Lederman, H.M., Ataxia-telangiectasia (A-T): an emerging dimension of premature ageing. Ageing Res. Rev., 2016, 10.1016/j.arr.2016.05.002.
9. [9] Watters, D.J., Oxidative stress in ataxia telangiectasia. Redox Rep. 8 (2003), 23–29, 10.1179/135100003125001206.
10. [10] Lavin, M.F., ATM: the product of the gene mutated in ataxia-telangiectasia. Int. J. Biochem. Cell Biol. 31 (1999), 735–740, 10.1016/S1357-2725(99)00028-X.
11. [11] Wu, Z.-H., Phenotypes and genotypes of the chromosomal instability syndromes. Transl. Pediatr. 5 (2016), 79–83, 10.21037/tp.2016.03.04.
12. [12] Valentin-Vega, Y.A., MacLean, K.H., Tait-Mulder, J., Milasta, S., Steeves, M., Dorsey, F.C., Cleveland, J.L., Green, D.R., Kastan, M.B., Mitochondrial dysfunction in ataxia-telangiectasia. Blood 119 (2012), 1490–1500, 10.1182/blood-2011-08-373639.
13. [13] Pallardó, F.V., Lloret, A., Lebel, M., D'Ischia, M., Cogger, V.C., Couteur, D.G. Le, Gadaleta, M.N., Castello, G., Pagano, G., Mitochondrial dysfunction in some oxidative stress-related genetic diseases: Ataxia-Telangiectasia, Down Syndrome, Fanconi Anaemia and Werner Syndrome. Biogerontology 11 (2010), 401–419, 10.1007/s10522-010-9269-4.
14. [14] Lee, S.-A., Lee, K.-M., Lee, S.-J., Yoo, K.-Y., Park, S.K., Noh, D.-Y., Ahn, S.-H., Kang, D., Antioxidant vitamins intake, ataxia telangiectasia mutated (ATM) genetic polymorphisms, and breast cancer risk. Nutr. Cancer 62 (2010), 1087–1094, 10.1080/01635581.2010.492088.
15. [15] Reliene, R., Schiestl, R.H., Experimental antioxidant therapy in ataxia telangiectasia., Clin. Med. Oncol. 2 (2008), 431–436.
16. [16] Reliene, R., Schiestl, R.H., Antioxidant N-acetyl cysteine reduces incidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair 5 (2006), 852–859, 10.1016/j.dnarep.2006.05.003.
17. [17] Pagano, G., Aiello Talamanca, A., Castello, G., Cordero, M.D., D'Ischia, M., Gadaleta, M.N., Pallardó, F.V., Petrović, S., Tiano, L., Zatterale, A., Oxidative stress and mitochondrial dysfunction across broad-ranging pathologies: toward mitochondria-targeted clinical strategies. Oxid. Med. Cell. Longev., 2014, 2014, 10.1155/2014/541230.
18. [18] Shiloh, Y., Tabor, E., Becker, Y., Abnormal response of ataxia-telangiectasia cells to agents that break the deoxyribose moiety of DNA via a targeted free radical mechanism. Carcinogenesis 4 (1983), 1317–1322, 10.1093/carcin/4.10.1317.
19. [19] Lavin, M.F., Scott, S., Gueven, N., Kozlov, S., Peng, C., Chen, P., Functional consequences of sequence alterations in the ATM gene. DNA Repair 3 (2004), 1197–1205, 10.1016/j.dnarep.2004.03.011.
20. [20] Lovejoy, C.A., Cortez, D., Common mechanisms of PIKK regulation. DNA Repair 8 (2009), 1004–1008, 10.1016/j.dnarep.2009.04.006.
21. [21] Chaudhary, M.W., Al-Baradie, R.S., Ataxia-telangiectasia: future prospects. Appl. Clin. Genet. 7 (2014), 159–167, 10.2147/TACG.S35759.
22. [22] Ambrose, M., Gatti, R.A., Pathogenesis of ataxia-telangiectasia: the next generation of ATM functions. Blood 121 (2013), 4036–4045, 10.1182/blood-2012-09-456897.
23. [23] Guo, Z., Deshpande, R., Paull, T.T., ATM activation in the presence of oxidative stress. Cell Cycle 9 (2010), 4805–4811, 10.4161/cc.9.24.14323.
24. [24] Guo, Z., Kozlov, S., Lavin, M.F., Person, M.D., Paull, T.T., ATM activation by oxidative stress (supp). Science 330 (2010), 517–521, 10.1126/science.1192912.
25. [25] Cosentino, C., Grieco, D., Costanzo, V., ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair. EMBO J. 30 (2011), 546–555, 10.1038/emboj.2010.330.
26. [26] Kobayashi, J., Saito, Y., Okui, M., Miwa, N., Komatsu, K., Increased oxidative stress in AOA3 cells disturbs ATM-dependent DNA damage responses. Mutat. Res. - Genet. Toxicol. Environ. Mutagen. 782 (2015), 42–50, 10.1016/j.mrgentox.2015.03.012.
27. [27] Lavin, M.F., Radiosensitivity and oxidative signalling in ataxia telangiectasia: an update. Radiother. Oncol. 47 (1998), 113–123, 10.1016/S0167-8140(98)00027-9.
28. [28] Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T.D., Mazur, M., Telser, J., Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007), 44–84, 10.1016/j.biocel.2006.07.001.
29. [29] Patel, M., Targeting Oxidative stress in central nervous system disorders. Trends Pharmacol. Sci., 2016, 10.1016/j.tips.2016.06.007.
30. [30] Klaunig, J.E., Wang, Z., Pu, X., Zhou, S., Oxidative stress and oxidative damage in chemical carcinogenesis. Toxicol. Appl. Pharmacol. 254 (2011), 86–99, 10.1016/j.taap.2009.11.028.
31. [31] Andreyev, A.Y., Kushnareva, Y.E., Starkov, A.A., Mitochondrial metabolism of reactive oxygen species. Biochem. Biokhimii︠a︡ 70 (2005), 200–214 〈http://www.ncbi.nlm.nih.gov/pubmed/15807660〉 (accessed 22.08.16).
32. [32] Bhat, A.H., Dar, K.B., Anees, S., Zargar, M.A., Masood, A., Sofi, M.A., Ganie, S.A., Oxidative stress, mitochondrial dysfunction and neurodegenerative diseases; a mechanistic insight. Biomed. Pharmacother. Bioméd. Pharm. 74 (2015), 101–110, 10.1016/j.biopha.2015.07.025.
33. [33] Yi, M., Rosin, M.P., Anderson, C.K., Response of fibroblast cultures patients to oxidative stress. Cancer 54 (1990), 43–50.
34. [34] Ward, A.J., Olive, P.L., Burr, A.H., Rosin, M.P., Response of fibroblast cultures from ataxia-telangiectasia patients to reactive oxygen species generated during inflammatory reactions. Environ. Mol. Mutagen. 24 (1994), 103–111, 10.1002/em.2850240205.
35. [35] Vuillaume, M., Reduced oxygen species, mutation, induction and cancer initiation. Mutat. Res. Genet. Toxicol. 186 (1987), 43–72, 10.1016/0165-1110(87)90014-5.
36. [36] Kasai, H., What causes human cancer? Approaches from the chemistry of DNA damage. Genes Environ. Off. J. Jpn. Environ. Mutagen Soc., 38, 2016, 19, 10.1186/s41021-016-0046-8.
37. [37] Chiesa, N., Barlow, C., Wynshaw-Boris, A., Strata, P., Tempia, F., Atm-deficient mice Purkinje cells show age-dependent defects in calcium spike bursts and calcium currents. Neuroscience 96 (2000), 575–583, 10.1016/S0306-4522(99)00581-3.
38. [38] A. Kamsler, D. Daily, A. Hochman, Increased oxidative stress in Ataxia Telangiectasia evidenced by alterations in redox state of brains from Atm-deficient Mice 1, 2001, pp. 1849–1854.
39. [39] Barlow, C., Dennery, P., Shigenaga, M., Smith, M., Morrow, J., Roberts, L., Wynshaw-Boris, A., Levine, R., Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs. Proc. Natl. Acad. Sci. 96 (1999), 9915–9919, 10.1073/pnas.96.17.9915.
40. [40] Biton, S., Barzilai, A., Shiloh, Y., The neurological phenotype of ataxia-telangiectasia: solving a persistent puzzle. DNA Repair 7 (2008), 1028–1038, 10.1016/j.dnarep.2008.03.006.
41. [41] Shackelford, R.E., Manuszak, R.P., Johnson, C.D., Hellrung, D.J., Link, C.J., Wang, S., Iron chelators increase the resistance of Ataxia telangeictasia cells to oxidative stress. DNA Repair 3 (2004), 1263–1272, 10.1016/j.dnarep.2004.01.015.
42. [42] Reichenbach, J., Schubert, R., Schindler, D., Müller, K., Böhles, H., Zielen, S., Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid. Redox Signal. 4 (2002), 465–469, 10.1089/15230860260196254.
43. [43] D'Souza, A.D., Parish, I.A., Krause, D.S., Kaech, S.M., Shadel, G.S., Reducing mitochondrial ROS improves disease-related pathology in a mouse model of ataxia-telangiectasia. Mol. Ther. 21 (2012), 42–48, 10.1038/mt.2012.203.
44. [44] Kalifa, L., Gewandter, J.S., Staversky, R.J., Sia, E.A., Brookes, P.S., O'Reilly, M.A., DNA double-strand breaks activate ATM independent of mitochondrial dysfunction in A549 cells. Free Radic. Biol. Med. 75 (2014), 30–39, 10.1016/j.freeradbiomed.2014.07.011.
45. [45] Resseguie, E.A., Staversky, R.J., Brookes, P.S., O'Reilly, M.A., Hyperoxia activates ATM independent from mitochondrial ROS and dysfunction. Redox Biol. 5 (2015), 176–185, 10.1016/j.redox.2015.04.012.
46. [46] Yu, J.H., Cho, S.O., Lim, J.W., Kim, N., Kim, H., Ataxia telangiectasia mutated inhibits oxidative stress-induced apoptosis by regulating heme oxygenase-1 expression. Int. J. Biochem. Cell Biol. 60 (2015), 147–156, 10.1016/j.biocel.2015.01.002.
47. [47] Semlitsch, M., Shackelford, R.E., Zirkl, S., Sattler, W., Malle, E., ATM protects against oxidative stress induced by oxidized low-density lipoprotein. DNA Repair 10 (2011), 848–860, 10.1016/j.dnarep.2011.05.004.
48. [48] Weyemi, U., Redon, C.E., Aziz, T., Choudhuri, R., Maeda, D., Parekh, P.R., Bonner, M.Y., Arbiser, J.L., Bonner, W.M., NADPH oxidase 4 is a critical mediator in Ataxia telangiectasia disease. Proc. Natl. Acad. Sci. 112 (2015), 2121–2126, 10.1073/pnas.1418139112.
49. [49] Guo, S., Chen, X., The human Nox4: gene, structure, physiological function and pathological significance. J. Drug Target. 23 (2015), 888–896, 10.3109/1061186X.2015.1036276.
50. [50] Reichenbach, J., Schubert, R., Schwan, C., Müller, K., Böhles, H.J., Zielen, S., Anti-oxidative capacity in patients with ataxia telangiectasia. Clin. Exp. Immunol. 117 (1999), 535–539, 10.1046/j.1365-2249.1999.01000.x.
51. [51] da Silva, R., dos Santos-Valente, E.C., Burim Scomparini, F., Saccardo Sarni, R.O., Costa-Carvalho, B.T., The relationship between nutritional status, vitamin A and zinc levels and oxidative stress in patients with ataxia-telangiectasia. Allergol. Immunopathol. 42 (2014), 329–335, 10.1016/j.aller.2013.02.013.
52. [52] Degan, P., d'Ischia, M., Pallardó, F.V., Zatterale, A., Brusco, A., Calzone, R., Cavalieri, S., Kavakli, K., Lloret, A., Manini, P., Pisanti, M.A., Vuttariello, E., Pagano, G., Glutathione levels in blood from ataxia telangiectasia patients suggest in vivo adaptive mechanisms to oxidative stress. Clin. Biochem. 40 (2007), 666–670, 10.1016/j.clinbiochem.2007.03.013.
53. [53] Lloret, A., Calzone, R., Dunster, C., Manini, P., d'Ischia, M., Degan, P., Kelly, F.J., Pallardó, F.V., Zatterale, A., Pagano, G., Different patterns of in vivo pro-oxidant states in a set of cancer- or aging-related genetic diseases. Free Radic. Biol. Med. 44 (2008), 495–503, 10.1016/j.freeradbiomed.2007.10.046.
54. [54] Aksoy, Y., Sanal, Ö., Metin, A., Tezcan, I., Ersoy, F., Öǧüş, H., Özer, N., Antioxidant enzymes in red blood cells and lymphocytes of ataxia-telangiectasia patients. Turk. J. Pediatr. 46 (2004), 204–207.
55. [55] Bitelo Ludwig, L., Valiati, V.H., Palazzo, R.P., Jardim, L.B., Da Rosa, D.P., Bona, S., Rodrigues, G., Marroni, N.P., Prá, D., Maluf, S.W., Chromosome instability and oxidative stress markers in patients with ataxia telangiectasia and their parents. Biomed. Res. Int., 2013, 2013, 10.1155/2013/762048.
56. [56] Chrzanowska, K.H., Gregorek, H., Dembowska-Bagińska, B., Kalina, M.A., Digweed, M., Nijmegen breakage syndrome (NBS). Orphanet J. Rare Dis., 7, 2012, 13, 10.1186/1750-1172-7-13.
57. [57] Digweed, M., Sperling, K., Nijmegen breakage syndrome: clinical manifestation of defective response to DNA double-strand breaks. DNA Repair 3 (2004), 1207–1217, 10.1016/j.dnarep.2004.03.004.
58. [58] Arora, H., Chacon, A.H., Choudhary, S., Mcleod, M.P., Meshkov, L., Nouri, K., Izakovic, J., Bloom syndrome. Int. J. Dermatol. 53 (2014), 798–802, 10.1111/ijd.12408.
59. [59] Krenzlin, H., Demuth, I., Salewsky, B., Wessendorf, P., Weidele, K., Bürkle, A., Digweed, M., DNA damage in nijmegen breakage syndrome cells leads to PARP hyperactivation and increased oxidative stress. PLoS Genet. 8 (2012), 1–8, 10.1371/journal.pgen.1002557.
60. [60] Kondratenko, I., Paschenko, O., Polyakov, A., Bologov, A., Nijmegen breakage syndrome. Adv. Exp. Med. Biol., 2007, 61–67, 10.1007/978-0-387-72005-0_6.
61. [61] Tauchi, H., Matsuura, S., Kobayashi, J., Sakamoto, S., Komatsu, K., Nijmegen breakage syndrome gene, NBS1, and molecular links to factors for genome stability. Oncogene 21 (2002), 8967–8980, 10.1038/sj.onc.1206136.
62. [62] Zatterale, A., Kelly, F.J., Degan, P., d'Ischia, M., Pallardó, F.V., Calzone, R., Dunster, C., Lloret, A., Manini, P., Coğulu, O., Kavakli, K., Pagano, G., Oxidative stress biomarkers in four Bloom syndrome (BS) patients and in their parents suggest in vivo redox abnormalities in BS phenotype. Clin. Biochem. 40 (2007), 1100–1103, 10.1016/j.clinbiochem.2007.06.003.
63. [63] T.M. Nicotera, J. Notaro, S. Notaro, J. Schumer, A.A. Sandberg, Elevated superoxide dismutase in bloom's syndrome: a genetic condition of oxidative stress, 1989, pp. 5239–5243.
64. [64] Krüger, L., Demuth, I., Neitzel, H., Varon, R., Sperling, K., Chrzanowska, K.H., Seemanova, E., Digweed, M., Cancer incidence in Nijmegen breakage syndrome is modulated by the amount of a variant NBS protein. Carcinogenesis 28 (2007), 107–111, 10.1093/carcin/bgl126.
65. [65] Melchers, A., Stöckl, L., Radszewski, J., Anders, M., Krenzlin, H., Kalischke, C., Scholz, R., Jordan, A., Nebrich, G., Klose, J., Sperling, K., Digweed, M., Demuth, I., A systematic proteomic study of irradiated DNA repair deficient Nbn-mice. PLoS One, 4, 2009, 10.1371/journal.pone.0005423.
66. [66] Shimura, T., Kobayashi, J., Komatsu, K., Kunugita, N., Severe mitochondrial damage associated with low-dose radiation sensitivity in ATM- and NBS1-deficient cells. Cell Cycle 15 (2016), 1099–1107, 10.1080/15384101.2016.1156276.
67. [67] Anichini, C., Lotti, F., Longini, M., Felici, C., Proietti, F., Buonocore, G., Antioxidant strategies in genetic syndromes with high neoplastic risk in infant age. Tumor. J. 100 (2014), 590–599, 10.1700/1778.19256.
68. [68] Schubert, R., Erker, L., Barlow, C., Yakushiji, H., Larson, D., Russo, A., Mitchell, J.B., Wynshaw-Boris, A., Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum. Mol. Genet. 13 (2004), 1793–1802, 10.1093/hmg/ddh189.
69. [69] Ito, K., Takubo, K., Arai, F., Satoh, H., Matsuoka, S., Ohmura, M., Naka, K., Azuma, M., Miyamoto, K., Hosokawa, K., Ikeda, Y., Mak, T.W., Suda, T., Hirao, A., Regulation of reactive oxygen species by Atm is essential for proper response to DNA double-strand breaks in lymphocytes. J. Immunol. 178 (2007), 103–110 〈http://www.ncbi.nlm.nih.gov/pubmed/17182545〉 (accessed 19.08.16).
70. [70] Berni, A., Meschini, R., Filippi, S., Palitti, F., De Amicis, A., Chessa, L., L-Carnitine enhances resistance to oxidative stress by reducing DNA damage in Ataxia telangiectasia cells. Mutat. Res. - Genet. Toxicol. Environ. Mutagen. 650 (2008), 165–174, 10.1016/j.mrgentox.2007.11.008.
71. [71] McDonald, C.J., Ostini, L., Wallace, D.F., John, A.N., Watters, D.J., Subramaniam, V.N., Iron loading and oxidative stress in the Atm-/- mouse liver. Am. J. Physiol. Gastrointest. Liver Physiol. 300 (2011), G554–G560, 10.1152/ajpgi.00486.2010.