The aspergillus nidulans ATM kinase regulates mitochondrial function, glucose uptake and the carbon starvation response

G3: Genes, Genomes, Genetics

Volumn 4, Issue 1, 2014, Pages 49-62

  Krohn, Nadia Graciele ^b   Brown, Neil Andrew ^b   Colabardini, Ana Cristina ^b   Reis, Thaila ^b   Savoldi, Marcela ^b   Dinamarco, Taísa Magnani ^b   Goldman, Maria Helena S ^b   Goldman, Gustavo Henrique ^a,b  

^a BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

ATM kinase; Autophagy; Cell death; Glucose starvation

Indexed keywords

ATM PROTEIN; CARBON; FUNGAL ENZYME; GLUCOSE; GLYOXYLIC ACID; HYDROLASE; PROTEINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR XPRG; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; AUTOPHAGY; CELL DIVISION; CELL ENERGY; CELL GROWTH; CELL METABOLISM; CONTROLLED STUDY; EMERICELLA NIDULANS; ENZYME RELEASE; GLUCOSE TRANSPORT; METABOLIC STRESS; MITOCHONDRION; MOLECULAR INTERACTION; NONHUMAN; NUTRIENT AVAILABILITY; OXIDATIVE PHOSPHORYLATION; PROTEIN FUNCTION; REGULATORY MECHANISM; STARVATION;

ATM KINASE; AUTOPHAGY; CELL DEATH; GLUCOSE STARVATION;

ASPERGILLUS NIDULANS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; AUTOPHAGY; CARBON; CELL CYCLE PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; GLYOXYLATES; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84892692636     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.008607     Document Type: Article

References (89)

1. Alexander, A., J. Kim, and C. L. Walker, 2010a ATM engages the TSC2/ mTORC1 signaling node to regulate autophagy. Autophagy 6: 672-673.
2. Ambrose, M., and R. A. Gatti, 2013 Pathogenesis of ataxia-telangiectasia: the next generation of ATM functions. Blood 121: 4036-4045.
3. Armata, H. L., D. Golebiowski, D. Y. Jung, H. J. Ko, J. K. Kim et al., 2010 Requirement of the ATM/p53 tumor suppressor pathway for glucose homeostasis. Mol. Cell. Biol. 30: 5787-5794.
4. Banin, S., S. Shieh, Y. Taya, C. W. Anderson, L. Chessa et al., 1998 Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281: 1674-1677.
5. Barbet, N. C., U. Schneider, S. B. Helliwell, I. Stansfield, M. F. Tuite et al., 1996 TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7: 25-42.
6. Barlow, C., K. D. Brown, C.-X. Deng, D. A. Tagle, and A. Wynshaw-Boris, 1997 Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17: 453-456.
7. Barlow, C., P. A. Dennery, M. K. Shigenaga, M. A. Smith, J. D. Morrow et al., 1999 Loss of the ataxiatelangiectasia gene product causes oxidative damage in target organs. Proc. Natl. Acad. Sci. USA 96: 9915-9919.
8. Barros, M. H., B. Bandy, E. B. Tahara, and A. J. Kowaltowski, 2004 Higher respiratory activity decreases mitochondrial reactive oxygen release and increases lifespan in Saccharomyces cerevisiae. J. Biol. Chem. 279: 49883-49888.
9. Bartkova, J., N. Rezaei, M. Liontos, P. Karakaidos, D. Kletsas et al., 2006 Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 444: 633-637.
10. Bensimon, A., R. Aebersold, and Y. Shiloh, 2011 Beyond ATM: The protein kinase landscape of the DNA damage response. FEBS Lett. 585: 1625-1639.
11. Boder, E., and R. P. Sedgwick, 1958 Ataxia-telangiectasia: a familial syndrome of progressive cerebellar ataxia, oculocutaneous telangiectasia and frequent pulmonary infection. Pediatrics 21: 526-554.
12. Brown, NA, P. F. de Gouve, N. G. Krohn, M. Savoldi, and G. H. Goldman, 2013 Functional characterisation of the non-essential protein kinases and phosphatases regulating Aspergillus nidulans hydrolytic enzyme production. Biotechnol. Biofuels 6: 91.
13. Bursch, W., A. Karwan, M. Mayer, J. Dornetshuber, U. Fröhwein et al., 2008 Cell death and autophagy: cytokines, drugs, and nutritional factors. Toxicology 254: 147-157.
14. Busti, S., P. Coccetti, L. Alberghina, and M. Vanoni, 2010 Glucose signalingmediated coordination of cell growth and cell cycle in Saccharomyces cerevisiae. Sensors (Basel Switzerland) 10: 6195-6240.
15. Canman, C. E., D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai et al., 1998 Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281: 1677-1679.
16. Ching, J. K., P. Rajguru, N. Marupudi, S. Banerjee, and J. S. Fisher, 2010 A role for AMPK in increased insulin action after serum starvation. Am. J. Physiol. Cell Physiol. 299: C1171-C1179.
17. Clutterbuck, A. J., 1993 Aspergillus nidulans (nuclear genes), pp. 3.71-3.84 in Locus Maps of Complex Genomes: Lower Eukaryotes, Vol. 3, edited byO'Brien, S. J., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
18. de Castro, P. A., M. Savoldi, D. Bonatto, M. H. Barros, M. H. S. Goldman et al., 2011 Molecular characterization of propolis-induced cell death in Saccharomyces cerevisiae. Eukaryot. Cell 10: 398-411.
19. Dechant, R., and M. Peter, 2008 Nutrient signals driving cell growth. Curr. Opin. Cell Biol. 20: 678-687.
20. Dementhon, K., G. Iyer, and N. L. Glass, 2006 VIB-1 is required for expression of genes necessary for programmed cell death in Neurospora. Eukaryot. Cell 5: 2161-2173.
21. Derheimer, F. A., and M. B. Kastan, 2010 Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett. 584: 3675-3681.
22. de Virgilio, C., and R. Loewith, 2006 Cell growth control: little eukaryotes make big contributions. Oncogene 25: 6392-6415.
23. Dinamarco, T. M., B. C. Pimentel Figueiredo, M. Savoldi, I. Malavazi, F. M. Soriani et al., 2010 The roles played by Aspergillus nidulans apoptosisinducing factor (AIF)-like mitochondrial oxidoreductase (AifA) and NADH-ubiquinone oxidoreductases (NdeA-B and NdiA) in farnesol resistance. Fungal Genet. Biol. 12: 1055-1069.
24. Ditch, S., and T. T. Paull, 2012 ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 37: 15-22.
25. Eaton, J. S., Z. P. Lin, A. C. Sartorelli, N. D. Bonawitz, and G. S. Shadel, 2007 Ataxia-telangiectasia mutated kinase regulates ribonucleotide reductase and mitochondrial homeostasis. J. Clin. Invest. 117: 2723-2734.
26. Emri, T., Z. Molnár, T. Pusztahelyi, and I. Pócsi, 2004 Physiological and morphological changes in autolysing Aspergillus nidulans cultures. Folia Microbiol. (Praha) 49: 277-284.
27. Emri, T., Z. Molnár, M. Szilágyi, and I. Pócsi, 2008 Regulation of autolysis in Aspergillus nidulans. Appl. Biochem. Biotechnol. 151: 211-220.
28. Fantes, P. A., and C. F. Roberts, 1973 Beta-galactosidase activity and lactose utilization in Aspergillus nidulans. J. Gen. Microbiol. 77: 417-486.
29. Fingar, D. C., and J. Blenis, 2004 Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23: 3151-3171.
30. Flipphi, M., J. Kocialkowska, and B. Felenbok, 2002 Characteristics of physiological inducers of the ethanol utilization (alc) pathway in Aspergillus nidulans. Biochem. J. 15: 25-31.
31. Gatei, M., D. Shkedy, K. K. Khanna, T. Uziel, Y. Shiloh et al., 2001 Ataxiatelangiectasia: chronic activation of damage-responsive functions is reduced by alpha-lipoic acid. Oncogene 20: 289-294.
32. Giorgio, M., M. Trinei, E. Migliaccio, and P. G. Pelicci, 2007 Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8: 722-728.
33. Gray, J. V., G. A. Petsko, G. C. Johnston, D. Ringe, R. A. Singer et al., 2004 'Sleeping beauty': quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 68: 187-206.
34. Halaby, M. J., J. C. Hibma, J. He, and A. N. D. D. Q. Yang, 2008 ATM protein kinase mediates full activation of Akt and regulates glucose transporter 4 translocation by insulin in muscle cells. Cell. Signal. 20: 1555-1563.
35. Hahn, J. S., and D. J. Thiele, 2004 Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase. J. Biol. Chem. 279: 5169-5176.
36. Inoki, K., T. Zhu, and K. L. Guan, 2003 TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590.
37. Jazwinski, S. M., 2013 The retrograde response: When mitochondrial quality control is not enough. Biochim. Biophys. Acta 1833: 400-409.
38. Kafer, E., 1977 Meiotic and mitotic recombination in Aspergilllus and its chromosomal aberrations. Adv. Genet. 19: 33-131.
39. Kamada, Y., T. Funakoshi, T. Shintani, K. Nagano, M. Ohsumi et al., 2000 Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150: 1507-1513.
40. Kamsler, A., D. Daily, A. Hochman, N. Stern, Y. Shiloh et al., 2001 Increased oxidative stress in ataxia telangiectasia evidenced by alterations in redox state of brains from Atm-deficient mice. Cancer Res. 61: 1849-1854.
41. Kang, M. Y., H.-B. Kim, C. Piao, K. H. Lee, J. W. Hyun et al., 2013 The critical role of catalase in prooxidant and antioxidant function of p53. Cell Death Differ. 20: 117-129.
42. Kastan, M. B., and D.-S. Lim, 2000 The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1: 179-186.
43. Katz, M. E., P. K. Flynn, P. A. vanKuyk, and B. F. Cheetham, 1996 Mutations affecting extracellular protease production in the filamentous fungus Aspergillus nidulans. Mol. Gen. Genet. 250: 715-724.
44. Katz, M. E., K.-A. Gray, and B. F. Cheetham, 2006 The Aspergillus nidulans xprG (phoG) gene encodes a putative transcriptional activator involved in the response to nutrient limitation. Fungal Genet. Biol. 43: 190-199.
45. Katz, M. E., C. J. Evans, E. E. Heagney, P. A. van Kuyk, J. M. Kelly et al., 2009 Mutations in genes encoding sorting nexins alter production of intracellular and extracellular proteases in Aspergillus nidulans. Genetics 181: 1239-1247.
46. Kershaw, M. J., and N. J. Talbot, 2009 Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc. Natl. Acad. Sci. USA 106: 15967-15972.
47. Ko, L. J., and C. Prives, 1996 p53: puzzle and paradigm. Genes Dev. 10: 1054-1072.
48. Kourtis, N., and N. Tavernarakis, 2009 Autophagy and cell death in model organisms. Cell Death Differ. 16: 21-30.
49. Langerak, P., and P. Russell, 2011 Regulatory networks integrating cell cycle control with DNA damage checkpoints and double-strand break repair. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366: 3562-3571.
50. Lavin, M. F., and Y. Shiloh, 1997 The genetic defect in ataxia-telangiectasia. Annu. Rev. Immunol. 15: 177-202.
51. Levine, A. J., 1997 p53, the cellular gatekeeper for growth and division. Cell 88: 323-331.
52. Levine, B., and G. Kroemer, 2008 Autophagy in the pathogenesis of disease. Cell 132: 27-42.
53. Liu, B., Y. Chen, and D. K. St Clair, 2008 ROS and p53: a versatile partnership. Free Radic. Biol. Med. 44: 1529-1535.
54. Malavazi, I., C. P. Semighini, M. R. Kress, S. D. Harris, and G. H. Goldman, 2006 Regulation of hyphal morphogenesis and the DNA damage response by the Aspergillus nidulans ATM homolog AtmA. Genetics 173: 99-109.
55. Malavazi, I., M. Savoldi, M. E. da Silva Ferreira, F. M. Soriani, P. S. Bonato et al., 2007 Transcriptome analysis of the Aspergillus nidulans AtmA (ATM, ataxia-telangiectasia) null mutant. Mol. Microbiol. 66: 74-99.
56. Malavazi, I., J. F. Lima, P. A. de Castro, M. Savoldi, W. de Souza et al., 2008 Genetic interactions of the Aspergillus nidulans atmAATM homolog with different components of the DNA damage response pathway. Genetics 178: 675-691.
57. Martinet, W., G. R. De Meyer, L. Andries, A. G. Herman, and M. M. Kockx, 2006 In situ detection of starvation-induced autophagy. J. Histochem. Cytochem. 54: 85-96.
58. Matsumoto, K., I. Uno, Y. Oshima, and T. Ishikawa, 1982 Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA 79: 2355- 2359.
59. Matsuoka, S., B. A. Ballif, A. Smogorzewska, E. R. McDonald, III, K. E. Hurov et al., 2007 ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166.
60. Mizushima, N., and D. J. Klionsky, 2007 Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 27: 19-40.
61. Mizushima, N., B. Levine, A. M. Cuervo, and D. J. Klionsky, 2008 Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075.
62. Nayak, T., E. Szewczyk, C. E. Oakley, A. Osmani, L. Ukil et al., 2006 A versatile and efficient gene targeting system for Aspergillus nidulans. Genetics 172: 1557-1566.
63. Nitsche, B. M., T. R. Joørgensen, M. Akeroyd, V. Meyer, and A. F. Ram, 2012 The carbon starvation response of Aspergillus niger during submerged cultivation: insights from the transcriptome and secretome. BMC Genomics 13: 380.
64. Oldham, S., and E. Hafen, 2003 Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol. 13: 79-85.
65. Oliveira, L. C. G., V. O. Silva, D. N. Okamoto, M. Y. Kondo, S. M. B. Santos et al., 2012 Internally quenched fluorescent peptide libraries with randomized sequences designed to detect endopeptidases. Anal. Biochem. 421: 299-307.
66. Osmani, S. A., G. S. May, and N. R. Morris, 1987 Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans. J. Cell Biol. 104: 1495-1504.
67. Patel, A. Y., T. M. McDonald, L. D. Spears, J. K. Ching, and J. S. Fisher, 2011 Ataxia telangiectasia mutated influences cytochrome c oxidase activity. Biochem. Biophys. Res. Commun. 405: 599-603.
68. Ramsdale, M., 2008 Programmed cell death in pathogenic fungi. Biochim. Biophys. Acta 1783: 1369-1380.
69. Rolland, F., J. H. de Winde, K. Lemaire, E. Boles, J. M. Thevelein et al., 2000 Glucose-induced cAMP signalling in yeast requires both a Gprotein coupled receptor system for extracellular glucose detection and a separable hexose kinase-dependent sensing process. Mol. Microbiol. 38: 348-358.
70. Rubio-Texeira, M., G. Van Zeebroeck, K. Voordeckers, and J. M. Thevelein, 2010 Saccharomyces cerevisiae plasma membrane nutrient sensors and their role in PKA signaling. FEMS Yeast Res. 10: 134-149.
71. Saito, S., A. A. Goodarzi, Y. Higashimoto, Y. Noda, S. P. Lees-Miller et al., 2002 ATM mediates phosphorylation at multiple p53 sites, including Ser46, in response to ionizing radiation. J. Biol. Chem. 277: 12491-12494.
72. Santos, J., C. Leão, and M. J. Sousa, 2012 Growth culture conditions and nutrient signaling modulating yeast chronological longevity. Oxid. Med. Cell Longev. 2012: 680-604
73. Semighini, C. P., M. Marins, M. H. S. Goldman, and G. H. Goldman, 2002 Quantitative analysis of the relative transcript levels of ABC transporter Atr genes in Aspergillus nidulans by real-time reverse transcription- PCR assay. Appl. Environ. Microbiol. 68: 1351-1357.
74. Sharon, A., A. Finkelstein, N. Shlezinger, and I. Hatam, 2009 Fungal apoptosis: function, genes and gene function. FEMS Microbiol. Rev. 33: 833-854.
75. Shiloh, Y., 2006 The ATM-mediated DNA-damage response: taking shape. Trends Biochem. Sci. 31: 402-410.
76. Stracker, T. H., I. Roig, P. A. Knobel, and M. Marjanovic, 2013 The ATM signaling network in development and disease. Front Genet. 4: 37.
77. Szilágyi, M., M. Miskei, Z. Karányi, B. Lenkey, I. Pócsi et al., 2013 Transcriptome changes initiated by carbon starvation in Aspergillus nidulans. Microbiology 159: 176-190.
78. Talbot, N. J., and M. J. Kershaw, 2009 The emerging role of autophagy in plant pathogen attack and host defense. Curr. Opin. Plant Biol. 12: 444- 450.
79. Valentin-Vega, Y. A., and M. B. Kastan, 2012 A new role for ATM: regulating mitochondrial function and mitophagy. Autophagy 8: 840-841.
80. Valentin-Vega, Y. A., K. H. Maclean, J. Tait-Mulder, S. Milasta, M. Steeves et al., 2012 Mitochondrial dysfunction in ataxia-telangiectasia. Blood 119: 1490-1500.
81. Vazquez-Martin, A., C. Oliveras-Ferraros, S. Cufí, B. Martin-Castillo, and J. A. Menendez, 2011 Metformin activates an ataxia telangiectasia mutated (ATM)/Chk2-regulated DNA damage-like response. Cell Cycle 10: 1499-1501.
82. Wang, J., J. C. Jiang, and S. M. Jazwinski, 2010 Gene regulation in yeast during life extension by nutrient limitation. Exp. Gerontol. 45: 621-631.
83. Wilson, W. A., and P. J. Roach, 2002 Nutrient-regulated protein kinases in budding yeast. Cell 111: 155-158.
84. Wullschleger, S., R. Loewith, and M. Hall, 2006 TOR signaling in growth and metabolism. Cell 124: 471-484.
85. Yanagisawa, S., T. Kikuma, and K. Kitamoto, 2013 Functional analysis of Aoatg1 and detection of the Cvt pathway in Aspergillus oryzae. FEMS Microbiol. Lett. 338: 168-176.
86. Yorimitsu, T., S. Zaman, J. R. Broach, and D. J. Klionsky, 2007 Protein kinase A and Sch9 cooperatively regulate induction of autophagy in Saccharomyces cerevisiae. Mol. Biol. Cell. 18(10): 4180-4189.
87. Zdralevic, M., N. Guaragnella, E. M. Antonacci, and S. Giannattasio, 2012 Yeast as a tool to study signaling pathways in mitochondrial stress response and cytoprotection. Sci. World J. 2012: 912147.
88. Zhan, H., T. Suzuki, K. Aizawa, K. Miyagawa, R. Nagai et al., 2010 Ataxia telangiectasia mutated (ATM)-mediated DNA damage response in oxidative stress-induced vascular endothelial cell senescence. J. Biol. Chem. 285: 29662-29670.
89. Zhao, M., and D. J. Klionsky, 2011 AMPK-dependent phosphorylation of ULK1 induces autophagy. Cell Metab. 13: 119-120.