Etoposide induces ATM-dependent mitochondrial biogenesis through AMPK activation

PLoS ONE

Volumn 3, Issue 4, 2008, Pages

  Fu, Xuan ^a,b   Wan, Shan ^a   Lyu, Yi Lisa ^a   Liu, Leroy F ^a   Qi, Haiyan ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ATM PROTEIN; ETOPOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN TFAM; THREONINE; TRANSCRIPTION FACTOR NRF1; 5 AMINO 4 IMIDAZOLECARBOXAMIDE; ACETYL COENZYME A CARBOXYLASE; AICA RIBONUCLEOTIDE; AMP ACTIVATED PROTEIN KINASES; AMP-ACTIVATED PROTEIN KINASES; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; DRUG DERIVATIVE; ENZYME INHIBITOR; HYDROGEN PEROXIDE; MULTIENZYME COMPLEX; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; RIBONUCLEOTIDE; TUMOR SUPPRESSOR PROTEIN;

ALPHA CHAIN; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DRUG ACTIVITY; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MITOCHONDRION; MONITORING; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; UPREGULATION; ANIMAL; CELL SURVIVAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL; PHOSPHORYLATION;

ATAXIA TELANGIECTASIA;

ACETYL-COA CARBOXYLASE; AMINOIMIDAZOLE CARBOXAMIDE; ANIMALS; CELL CYCLE PROTEINS; CELL SURVIVAL; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ENZYME INHIBITORS; ETOPOSIDE; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MULTIENZYME COMPLEXES; NEURONS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RIBONUCLEOTIDES; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 44349184864     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002009     Document Type: Article

References (90)

1. Taylor RW, Turnbull DM (2005) Mitochondrial DNA mutations in human disease. Nat Rev Genet 6: 389-402.
2. Zeviani M, Carelli V (2003) Mitochondrial disorders. Curt Opin Neural 16: 585-594.
3. Sadun AA, Carelli V (2003) Mitochondrial function and dysfunction within the optic nerve. Arch Ophthalmol 121: 1342-1343.
4. Zeviani M, Spinazzola A, Carelli V (2003) Nuclear genes in mitochondrial disorders. Curr Opin Genet Dev 13: 262-270.
5. Scarpulla RC (2006) Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem 97: 673-683.
6. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
7. Virbasius JV, Scarpulla RC (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci U S A 91: 1309 1313.
8. Gleyzer N, Vercauteren K, Scarpulla RC (2005) Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol Cell Biol 25: 1354-1366.
9. Lowell BB, Spiegelman BM (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404: 652-660.
10. Clayton DA (1992) Transcription and replication of animal mitochondrial DNAs. Int Rev Cytol 141: 217-232.
11. Reznick RM, Shulman GI (2006) The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 574: 33-39.
12. Zong H, Ren JM, Young LH, Pypaert M, Mu J, et al. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99: 15983-15987.
13. Bergeron R, Ren JM, Cadman KS, Moore IK, Perret P, et al. (2001) Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am J Physiol Endocrinol Metab 281: E1340-1346.
14. Hong SP, Leiper FC, Woods A, Carling D, Carlson M (2003) Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci U S A 100: 8839-8843.
15. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, et al. (2005) The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 280: 29060-29066.
16. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, et al. (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296: 349-352.
17. Woods A, Johnstane SR, Dickerson K, Leiper FC, Fryer LG, et al. (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13: 2004-2008.
18. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, et al. (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2: 9-19.
19. Hardie DG, Hawley SA, Scott JW (2006) AMP-activated protein kinase-development of the energy sensor concept. J Physiol 574: 7-15.
20. Jager S, Handschin C, St-Pierre J, Spirgelman BM (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 104: 12017-12022.
21. Kluza J, Marchetti P, Gallego MA, Lancel S, Fournier C, et al. (2004) Mitochondrial proliferation during apoptosis induced by anticancer agents: effects of doxorubicin and mitoxantrone on cancer and cardiac cells. Oncogene 23: 7018-7030.
22. Reipert S, Berry J, Hughes MF, Hickman JA, Allen TD (1995) Changes of mitochondrial mass in the hemopoictic stem cell line FDCP-mix after treatment with etoposide: a correlative study by multiparameter flow cytometry and confocal and electron microscopy. Exp Cell Res 221: 281-288.
23. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, et al. (1995) A single ataxia telangiectasia gene with a product similar to P1-3 kinase. Science 268: 1749-1753.
24. Zhang N, Chen P, Khanna KK, Scott S, Gatei M, et al. (1997) Isolation of full-length ATM cDNA and correction of the ataxia-telangiectasia cellular phenotype. Proc Natl Acad Sci U S A 94: 8021-8026.
25. Suzuki A, Kusakai G, Kishimoto A, Shimojo Y, Ogura T, et al. (2004) IGF-1 phosphorylates AMPK-alpha subunit in ATM-dependent and LKB1-independent manner. Biochem Biophys Res Commun 324: 986-992.
26. Sun Y, Connors KE, Yang DQ (2007) AICAR induces phosphorylation of AMPK in an ATM-dependent, LKB1-independent manner. Mol Cell Biochem 306: 239-245.
27. Tanaka T, Halicka HD, Traganos F, Seiter K, Darzynkiewicz Z (2007) Induction of ATM activation, historic H2AX phosphorylation and apoptosis by etoposide: relation to cell cycle phase. Cell Cycle 6: 371-376.
28. Zhang A, Lyn YL, Lin CP, Zhou N, Azarova AM, et al. (2006) A protease pathway for the repair of topoisomerase II-DNA covalent complexes. J Biol Chem 281: 35997-36003.
29. Kanki T, Ohgaki K, Gaspari M, Gustafsson CM, Fukuoh A, et al. (2004) Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol Cell Biol 24: 9823-9834.
30. Karpinich NO, Tafani M, Rothman RJ, Russo MA, Father JL (2002) The course of etoposide-induced apoptosis from damage to DNA and p53 activation to mitochondrial release of cytochrome c. J Biol Chem 277: 16547-16552.
31. Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, et al. (2004) Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc Natl Acad Sci U S A 101: 16507-16512.
32. Xu J, Shi C, Li Q, Wu J, Forster EL, et al. (2007) Mitochondrial dysfunction in platelets and hippocampi of senescence-accelerated mice. J Bioenerg Biomembr 39: 195-202.
33. Mathur A, Hong Y, Kemp BK, Barrientos AA, Erusalimisky JD (2000) Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes. Cardiovasc Res 46: 126-138.
34. Ambrose M, Goldstine JV, Gatti RA (2007) Intrinsic mitochondrial dysfunction in ATM-deficient lymphoblastoid cells. Hum Mol Genet.
35. Eaton JS, Lin ZP, Sartorelli AC, Bonawitz ND, Shadel GS (2007) Ataxiatelangiectasia mutated kinase regulates ribonucleotide reductase and mitochondrial homeostasis. J Clin Invest 117: 2723-2734.
36. Zhou G, Myers R, Li Y, Chen Y, Shen X, et al. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174.
37. Corton JM, Gillespie JG, Hawley SA, Hardic DG (1995) 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 229: 558-565.
38. Sullivan JE, Brocklehurst KJ, Marley AE, Carey F, Carling D, et al. (1994) Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett 353: 33-36.
39. Verdun RE, Crabbe L, Haggblom C, Karlseder J (2005) Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol Cell 20: 551-561.
40. Gui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, et al. (2006) Transcriptional repression of PGC-lalpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127: 59-69.
41. Chen H, McCaffery JM, Chan DC (2007) Mitochondrial Fusion Protects against Neurodegeneration in the Cerebellum. Cell 130: 548-562.
42. Chang DT, Reynolds IJ (2006) Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neumbiol 80: 241-268.
43. Lee CF, Liu CY, Hsieh RH, Wei YH (2005) Oxidative stress-induced depolymerization of microtubules and alteration of mitochondrial mass in human cells. Ann N Y Acad Sci 1042: 246-254.
44. Tanizawa A, Kubota M, Hashimoto H, Shimizu T, Takimoto T, et al. (1989) VP-16-induced nucleotide pool changes and poly(ADP-ribose) synthesis: the role of VP-16 in interphase death. Exp Cell Res 185: 237-246.
45. Barbe J, Villaverde A, Guerrero R (1983) Evolution of cellular ATP concentration after UV-mediated induction of SOS system in Escherichia coli. Biochem Biophys Res Common 117: 556-561.
46. Guerrero R, Llagostera M, Villaverde A, Barbe J (1984) Changes in ATP concentration in Escherichia coli during induction of the SOS system by mitomycin C and bleomycin. J Gen Microbiol 130: 2247-2251.
47. Marecki JC, McCord JM (2002) The inhibition of poly(ADP-ribose) polymerase enhances growth rates of ataxia telangiectasia cells. Arch Biochem Biophys 402: 227-234.
48. Chun HH, Gatti RA (2004) Ataxia-telangiectasia, an evolving phenotype. DNA Repair (Amst) 3: 1187-1196.
49. Gatti RA, Boder E, Vinters HV, Sparkes RS, Norman A, et al. (1991) Ataxia-telangiectasia: an interdisciplinary approach to pathogenesis. Medicine (Baltimore) 70: 99-117.
50. Boder E (1985) Ataxia-telangiectasia, Genetics, Neuropathology, and Inummology of a Degenerative Disease of Childhood. pp 1-63.
51. Tavani F, Zimmerman RA, Berry GT, Sullivan K, Gatti R, et al. (2003) Ataxia-telangiectasia: the pattern of cerebellar atrophy on MRI. Neuroradiology 45: 315-319.
52. Ammann AJ, Hong R (1971) Autoimmune phenomena in ataxia telangiectasia. J Pediatr 78: 821-826.
53. McFarlin DE, Strober W, Barlow M, Waldmann T (197 1) The immunological deficiency state in ataxia-telangiectasia. Res Pobl Assoc Res Nerv Merit Dis 49: 275-292.
54. Pan Q Petit-Frere C, Lahdesmaki A, Gregorck H, Chrzanowska KH, et al. (2002) Alternative end joining during switch recombination in patients with ataida-telangiectasia. Eur J Immunol 32: 1300-1308.
55. Morrell D, Chase CL, Swift M (1990) Cancers in 44 families with ataxia-telangiectasia. Cancer Genet Cytogenct 50: 119-123.
56. Swift M, Chase CL, Morrell D (1990) Cancer predisposition of ataxia-telangiectasia heterozygotes. Cancer Genet Cytogenet 46: 21-27.
57. Morrell D, Cromartie E, Swift M (1986) Mortality and cancer incidence in 263 patients with ataxia-telangiectasia. J Natl Cancer Inst 77: 89-92.
58. Taylor AM, Metcalfe JA, Thick J, Mak YF (1996) Leukemia and lymphoma in ataxia telangiectasia. Blood 87: 423-438.
59. Shiloh Y (1997) Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart. Annu Rev Genet 31: 635-662.
60. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, et al. (1996) Atmdeficient mice: a paradigm of ataxia telangiectasia. Cell 86: 159-171.
61. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, et al. (1996) Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci U S A 93: 13084-13089.
62. Bar RS, Levis WR, Rechler MM, Harrison LC, Siebert C, et al. (1978) Extreme insulin resistance in ataxia telangiectasia: defect in affinity of insulin receptors. N Engl J Med 298: 1164-1171.
63. Gotoff SP, Amirmokri E, Liebner EJ (1967) Ataxia telangiectasia. Neoplasia, untoward response to x-irradiation, and tuberous sclerosis. Am J Dis Child 114: 617-625.
64. Morgan JL, Holcomb TM, Morrissey RW (1968) Radiation reaction in ataxia telangiectasia. Am J Dis Child 116: 557-558.
65. Taylor AM, Harnden DG, Arlett CF, Harcourt SA, Lehmann AR, et al. (1975) Ataxia telangiectasia: a human mutation with abnormal radiation sensitivity. Nature 258: 427-429.
66. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506.
67. Kastan MB, Lim DS (2000) The many substrates and functions of ATM. Nat Rev Mol Cell Biol 1: 179-186.
68. Abraham RT (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15: 2177-2196.
69. Shiloh Y (2006) The ATM-mediated DNA-damage response: taking shape. Trends Biochem Sci 31: 402-410.
70. Barzilai A, Rotman G, Shiloh Y (2002) ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage. DNA Repair (Amst) 1: 3-25.
71. Reichenbach, Schubert, Schwan, Muller, Robles, et al. (1999) Anti-oxidative capacity in patients with ataxia telangiectasia. Clinical and Experimental Immunology 117: 535-539.
72. Reichenbach J, Schubert R, Schindler D, Muller K, Bohles H, et al. (2002) Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid Redox Signal 4: 465-469.
73. Ito K, Takubo K, Arai F, Satoh H, Matsuoka S, et al. (2007) Regulation of reactive oxygen species by Atm is essential for proper response to DNA double-strand breaks in lymphocytes. J Immunol 178: 103-110.
74. Reliene R, Fischer E, Schiestl RH (2004) Effect of N-acetyl cysteine on oxidative DNA damage and the frequency of DNA deletions in atm-deficient mice. Cancer Res 64: 5148-5153.
75. Quick KL, Dugan LL (2001) Superoxide stress identifies neurons at risk in a model of ataxia-telangiectasia. Ann Neurol 49: 627-635.
76. Barlow C, Dennery PA, Shigenaga MR, Smith MA, Morrow JD, et al. (1999) Loss of the ataxia-telangiectasia gene product causes oxidative damage in target organs. Proc Natl Acad Sci U S A 96: 9915-9919.
77. Meredith MJ, Dodson ML (1987) Imparied glutathione biosynthesis in cultured human ataxia-telangiectasia cells. Cancer Res 47: 4576-4581.
78. Browne SE, Roberts LJ 2nd, Dennery PA, Doctrow SR, Beal MF, et al. (2004) Treatment with a catalytic antioxidant corrects the neurobehavioral defect in ataxia-telangiectasia mice. Free Radic Biol Med 36: 938-942.
79. Reliene R, Schiestl RH (2006) Antioxidant N-acetyl cysteine reduces incidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair (Amst) 5: 852-859.
80. Schubert R, Erker L, Barlow C, Yakushji H, Larson D, et al, (2004) Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum Mol Genet 13: 1793-1802.
81. Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, et al. (2004) Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431: 997-1002.
82. Zhang Y, Qi H, Taylor R, Xu W, Liu LF, et al. (2007) The Role of Autophagy in Mitochondria Maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3: 337-346.
83. Tyagi A, Singh RP, Agarwal C, Siriwardana S, Sclafani RA, et al. (2005) Resveratrol causes Cdc2-tyr15 phosphorylation via ATM/ATR-Ghk1/2-Cdc25C pathway as a central mechanism for S phase arrest in human ovarian carcinoma Ovcar-3 cells. Carcinogenesis 26: 1978-1987.
84. Miyoshi N, Uchida K, Osawa T, Nakamura Y (2007) Selective cytotoxicity of benzyl isothiocyanate in the proliferating fibroblastoid cells. Int J Cancer 120: 484-492.
85. Zhou N, Xiao H, Li TK, Nur EKA, Liu LF (2003) DNA damage-mediated apoptosis induced by selenium compounds. J Biol Chem 278: 29532-29537.
86. Ziv Y, Bar-Shira A, Pecker I, Russell P, Jorgensen TJ, et al. (1997) Recombinant ATM protein complements the cellular A-T phenotype. Oncogene 15: 159-167.
87. Chen S, Wang G, Makrigiorgos GM, Price BD (2004) Stable siRNA-mediated silencing of ATM alters the transcriptional profile of HeLa cells. Biochem Biophys Res Commum 317: 1037-1044.
88. Gilad S, Bar-Shira A, Harnik R, Shkedy D, Ziv Y, et al. (1996) Ataxia-telangiectasia: founder effect among north African Jews. Hum Mol Genet 5: 2033-2037.
89. Meiners S, Nur-e-Kamal MS, Mercado ML (2001) Identification of a neurite outgrowth-promoting motif within the alternatively spliced region of human tenascin-C. J Neurosci 21: 7215-7225.
90. Qi H, Lin C, Fu X, Wood LM, Liu AA, et al. (2006) G-Quadruplexes Induce ATM/JNK-Dependent Apoptosis. Cancer Res 66.