Ataxia-telangiectasia mutated kinase in the control of oxidative stress, mitochondria, and autophagy in cancer: A maestro with a large orchestra

Frontiers in Oncology

Volumn 8, Issue MAR, 2018, Pages

  Stagni, Venturina ^a,b   Cirotti, Claudia ^a,b   Barilà, Daniela ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Ataxia telangiectasia mutated kinase; Cancer; Mitophagy autophagy; Oxidative stress; Proteostasis

Indexed keywords

EID: 85044384170     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2018.00073     Document Type: Short Survey

References (56)

1. Jones DP. Redefining oxidative stress. Antioxid Redox Signal (2006) 10:1865-79. doi:10.1089/ars.2006.8.1865
2. Poprac P, Jomova K, Simunkova M, Kollar V, Rhodes CJ, Valko M. Targeting free radicals in oxidative stress-related human diseases. Pharmacol Sci (2017) 38:592-607. doi:10.1016/j.tips.2017.04.005
3. Holmström KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol (2014) 15:411-21. doi:10.1038/nrm3801
4. Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J (2012) 5:9-19. doi:10.1097/WOX.0b013e3182439613
5. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev (2007) 87:245-313. doi:10.1152/physrev.00044.2005
6. Reichmann D, Voth W, Jakob U. Maintaining a healthy proteome during oxidative stress. Mol Cell (2018) 69:203-13. doi:10.1016/j.molcel.2017.12.021
7. Liang Y, Sigrist S. Autophagy and proteostasis in the control of synapse aging and disease. Curr Opin Neurobiol (2017) 48:113-21. doi:10.1016/j.conb.2017.12.006
8. Ciechanover A, Kwon TK. Protein quality control by molecular chaperones in neurodegeneration. Front Neurosci (2017) 11:185. doi:10.3389/fnins.2017.00185
9. Niforou K, Cheimonidou C, Trougakos IP. Molecular chaperones and proteostasis regulation during redox imbalance. Redox Biol (2014) 2:323-32. doi:10.1016/j.redox.2014.01.017
10. Hetz C, Papa FR. The unfolded protein response and cell fate control. Mol Cell (2018) 69:169-81. doi:10.1016/j.molcel.2017.06.017
11. Shiloh Y, Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat Rev Mol Cell Biol (2013) 14:197-210. doi:10.1038/nrm3546
12. Kamsler A, Daily D, Hochman A, Stern N, Shiloh Y, Rotman G, et al. Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res (2001) 61:1849-54
13. Reichenbach J, Schubert R, Schindler D, Müller K, Böhles H, Zielen S. Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid Redox Signal (2002) 4:465-9. doi:10.1089/15230860260196254
14. Shiloh Y, Lederman HM. Ataxia-telangiectasia (A-T): an emerging dimension of premature ageing. Ageing Res Rev (2017) 33:76-88. doi:10.1016/j.arr.2016.05.002
15. Valentin-Vega YA, MacLean KH, Tait-Mulder J, Milasta S, Steeves M, Dorsey FC, et al. Mitochondrial dysfunction in ataxia-telangiectasia. Blood (2012) 119:1490-500. doi:10.1182/blood-2011-08-373639
16. Ditch S, Paull TT. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem Sci (2012) 37:15-22. doi:10.1016/j.tibs.2011.10.002
17. Choy KR, Watters DJ. Neurodegeneration in ataxia-telangiectasia: multiple roles of ATM kinase in cellular homeostasis. Dev Dyn (2018) 247:33-46. doi:10.1002/dvdy.24522
18. Schubert R, Erker L, Barlow C, Yakushiji H, Larson D, Russo A, et al. Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum Mol Genet (2004) 13:1793-802. doi:10.1093/hmg/ddh189
19. Guo Z, Deshpande R, Paull TT. ATM activation in the presence of oxidative stress. Cell Cycle (2010) 9:4805-11. doi:10.4161/cc.9.24.14323
20. Cosentino C, Grieco D, Costanzo A. ATM activates the pentose phosphate pathway promoting anti-oxidant defence and DNA repair. EMBO J (2011) 30:546-55. doi:10.1038/emboj.2010.330
21. Ambrose M, Goldstine JV, Gatti RA. Intrinsic mitochondrial dysfunction in ATM-deficient lymphoblastoid cells. Hum Mol Genet (2007) 16:2154-64. doi:10.1093/hmg/ddm166
22. Alexander A, Cai S-L, Kim J, Nanez A, Sahin M, MacLean KH, et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci U S A (2010) 107:4153-8. doi:10.1073/pnas.0913860107
23. Zhang J, Tripathi DN, Jing J, Alexander A, Kim J, Powell RT, et al. ATM functions at the peroxisome to induce pexophagy in response to ROS. Nat Cell Biol (2015) 17:1259-69. doi:10.1038/ncb3230
24. Lee JH, Mand MR, Kao CH, Zhou Y, Ryu SW, Richards AL, et al. ATM directs DNA damage responses and proteostasis via genetically separable pathways. Sci Signal (2018) 11:eaan5598. doi:10.1126/scisignal.aan5598
25. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stressresponse. Mol Cell (2010) 40: 280-93. doi:10.1016/j.molcel.2010.09.023
26. Bhatti S, Kozlov S, Farooqi AA, Naqui A, Lavin MF, Khanna KK. ATM protein kinase: the linchpin of cellular defenses to stress. Cell Mol Life Sci (2011) 68:2977-3006. doi:10.1007/s00018-011-0683-9
27. Tripathi DN, Chowdhury R, Trudel LJ, Tee AR, Slack RS, Walker CL, et al. Reactive nitrogen species regulate autophagy through ATM-AMPK-TSC2-mediated suppression of mTORC1. Proc Natl Acad Sci U S A (2013) 110:E2950-7. doi:10.1073/pnas.1307736110
28. Cam H, Easton J, High A, Houghton P. mTORC1 signaling under hypoxic conditions is controlled by ATM-dependent phosphorylation of HIF-1a. Mol Cell (2010) 40:509-20. doi:10.1016/j.molcel.2010.10.030
29. Ousset M, Bouquet F, Fallone F, Biard D, Dray C, Vlet P, et al. Loss of ATM positively regulates the expression of hypoxia inducible factor 1 (HIF-1) through oxidative stress: role in the physiopathology of the disease. Cell Cycle (2010) 9:2814-22. doi:10.4161/cc.9.14.12253
30. Mongiardi P, Stagni V, Natoli M, Giaccari D, D'Agnano I, Falchetti M, et al. Oxygen sensing is impaired in ATM defective cells. Cell Cycle (2011) 10:4311-20. doi:10.4161/cc.10.24.18663
31. Antonelli M, Strappazzon F, Arisi I, Brandi R, D'Onofrio M, Sambucci M, et al. ATM kinase sustains breast cancer stem-like cells by promoting ATG4C expression and autophagy. Oncotarget (2017) 8:21692-709. doi:10.18632/oncotarget.15537
32. Wu T, Harder BG, Wong PK, Lang JE, Zhang DD. Oxidative stress, mammospheres and Nrf2-new implication for breast cancer therapy? Mol Carcinog (2015) 54:1494-502. doi:10.1002/mc.22202
33. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J (2007) 26:1749-60. doi:10.1038/sj.emboj.7601623
34. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J (2009) 417:1-13. doi:10.1042/BJ20081386
35. Schrader M, Fahimi HD. Peroxisomes and oxidative stress. Biochim Biophys Acta (2006) 1763:1755-66. doi:10.1016/j.bbamcr.2006.09.006
36. Watters D, Kedar P, Spring K, Bjorkman J, Chen P, Gatei M, et al. Localization of a portion of extranuclear ATM to peroxisomes. J Biol Chem (1999) 274:34277-82. doi:10.1074/jbc.274.48.34277
37. Fang EF, Kassahun H, Croteau DL, Scheibye-Knudsen M, Marosi K, Lu H, et al. NAD+ replenishment improves lifespan and healthspan in ataxia telangiectasia models via mitophagy and DNA repair. Cell Metab (2016) 24:566-81. doi:10.1016/j.cmet.2016.09.004
38. Qi Y, Qiu Q, Gu X, Tian Y, Zhang Y. ATM mediates spermidine-induced mitophagy via PINK1 and Parkin regulation in human fibroblasts. Sci Rep (2016) 6:24700. doi:10.1038/srep24700
39. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov (2009) 8:579-91. doi:10.1038/nrd2803
40. Panieri E, Santoro MM. ROS homeostasis and metabolism: a dangerous liason in cancer cells. Cell Death Dis (2016) 7:e2253. doi:10.1038/cddis.2016.105
41. Gào X, Schöttker B. Reduction-oxidation pathways involved in cancer development: a systematic review of literature reviews. Oncotarget (2017) 8:51888-906. doi:10.18632/oncotarget.17128
42. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res (2010) 44:479-96. doi:10.3109/10715761003667554
43. Deshaies RJ. Proteotoxic crisis, the ubiquitin-proteasome system, and cancer therapy. BMC Biol (2014) 12:94. doi:10.1186/s12915-014-0094-0
44. Rappa F, Farina F, Zummo G, David S, Campanella C, Carini F, et al. HSP-molecular chaperones in cancer biogenesis and tumor therapy: an overview. Anticancer Res (2012) 32:5139-50
45. Neckers L, Workman P. Hsp90 molecular chaperone inhibitors: are we there yet? Clin Cancer Res (2012) 18:64-76. doi:10.1158/1078-0432.CCR-11-1000
46. Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT. ATM activation by oxidative stress. Science (2010) 330:517-21. doi:10.1126/science.1192912
47. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, et al. Autophagy in malignant transformation and cancer progression. EMBO J (2015) 34:856-80. doi:10.15252/embj.201490784
48. Rodolfo C, Di Bartolomeo S, Cecconi F. Autophagy in stem and progenitor cells. Cell Mol Life Sci (2016) 73:475-96. doi:10.1007/s00018-015-2071-3
49. Maycotte P, Jones KL, Goodall ML, Thorburn J, Thorburn A. Autophagy supports breast cancer stem cell maintenance by regulating IL6 secretion. Mol Cancer Res (2015) 13:651-8. doi:10.1158/1541-7786.MCR-14-0487
50. Wolf J, Dewi DL, Fredebohm J, Müller-Decker K, Flechtenmacher C, Hoheisel JD, et al. A mammosphere formation RNAi screen reveals that ATG4A promotes a breast cancer stem-like phenotype. Cancer Res (2013) 15:R109. doi:10.1186/bcr3576
51. Gong C, Bauvy C, Tonelli G, Yue W, Deloménie C, Nicolas V, et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene (2013) 32:2261-72. doi:10.1038/onc.2012.252
52. Jhaveri K, Ochiana SO, Dunphy MP, Gerecitano JF, Corben AD, Peter RI, et al. Heat shock protein 90 inhibitors in the treatment of cancer: current status and future directions. Expert Opin Investig Drugs (2014) 23:611-28. doi:10.1517/13543784.2014.902442
53. Matsuoka S, Ballif B, Smogorzewska A, McDonald E 3rd, Hurov K, Luo JL, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science (2007) 316:1160-6. doi:10.1126/science.1140321
54. Elaimy AL, Ahsan A, Marsh K, Pratt WB, Ray D, Lawrence TS, et al. ATM is the primary kinase responsible for phosphorylation of Hsp90a after ionizing radiation. Oncotarget (2016) 7:82450-7. doi:10.18632/oncotarget.12557
55. Stagni V, Manni I, Oropallo V, Mottolese M, Di Benedetto A, Piaggio G, et al. ATM kinase sustains HER2 tumorigenicity in breast cancer. Nat Commun (2015) 16(6):6886. doi:10.1038/ncomms7886
56. Stagni V, Oropallo V, Barilà D. ATM: an unexpected tumor-promoting factor in HER2-expressing tumors. Mol Cell Oncol (2015) 3:e1054551. doi:10.1080/23723556.2015.1054551