Iron deprivation induces transcriptional regulation of mitochondrial biogenesis

Journal of Biological Chemistry

Volumn 291, Issue 40, 2016, Pages 20827-20837

  Rensvold, Jarred W ^a   Krautkramer, Kimberly A ^b   Dowell, James A ^b   Denu, John M ^a,b   Pagliarini, David J ^a,c  

^a MORGRIDGE INSTITUTE FOR RESEARCH   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; ALKYLATION; BIOSYNTHESIS; ENCODING (SYMBOLS); GENES; MASS SPECTROMETRY; MITOCHONDRIA; NUTRIENTS; PROTEINS; TRANSCRIPTION;

ENVIRONMENTAL CHANGE; EPIGENETIC ALTERATIONS; HISTONE DEACETYLASES; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL PROTEIN; TRANSCRIPTIONAL CHANGES; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REPRESSION;

IRON;

HISTONE DEACETYLASE; MITOCHONDRIAL PROTEIN; HISTONE; IRON;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; IRON DEPRIVATION; IRON METABOLISM; LIMIT OF QUANTITATION; MASS SPECTROMETRY; MITOCHONDRIAL BIOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; ACETYLATION; ANIMAL; BIOSYNTHESIS; DEFICIENCY; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; METABOLISM; MUSCLE MITOCHONDRION;

ACETYLATION; ANIMALS; EPIGENESIS, GENETIC; HISTONES; IRON; MICE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84988960200     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.727701     Document Type: Article

References (62)

1. Quirós, P. M., Langer, T., and López-Otín, C. (2015) New roles for mitochondrial proteases in health, ageing and disease. Nat. Rev. Mol. Cell Biol. 16, 345-359
2. Labbé, K., Murley, A., and Nunnari, J. (2014) Determinants and functions of mitochondrial behavior. Annu. Rev. Cell Dev. Biol. 30, 357-391
3. Scarpulla, R. C., Vega, R. B., and Kelly, D. P. (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab. 23, 459-466
4. Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., Ong, S. E., Walford, G. A., Sugiana, C., Boneh, A., Chen, W. K., Hill, D. E., Vidal, M., Evans, J. G., Thorburn, D. R., Carr, S. A., and Mootha, V. K. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123
5. Calvo, S. E., Clauser, K. R., and Mootha, V. K. (2016) MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins. Nucleic Acids Res. 44, D1251-D1257
6. DiMauro, S., and Schon, E. A. (2003) Mitochondrial respiratory-chain diseases. N. Engl. J. Med. 348, 2656-2668
7. Lowell, B. B., and Shulman, G. I. (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307, 384-387
8. Vafai, S. B., and Mootha, V. K. (2012) Mitochondrial disorders as windows into an ancient organelle. Nature 491, 374-383
9. Wallace, D. C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407
10. Wallace, D. C. (1999) Mitochondrial diseases in man and mouse. Science 283, 1482-1488
11. Goldenthal, M. J., and Marín-García, J. (2004) Mitochondrial signaling pathways: a receiver/integrator organelle. Mol. Cell Biochem. 262, 1-16
12. Hock, M. B., and Kralli, A. (2009) Transcriptional control of mitochondrial biogenesis and function. Annu. Rev. Physiol. 71, 177-203
13. Wallace, D. C., and Fan, W. (2010) Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10, 12-31
14. Frey, P. A., and Reed, G. H. (2012) The ubiquity of iron. ACS Chem. Biol. 7, 1477-1481
15. Mense, S. M., and Zhang, L. (2006) Heme: a versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res. 16, 681-692
16. Rouault, T. A. (2015) Iron-sulfur proteins hiding in plain sight. Nat. Chem. Biol. 11, 442-445
17. Richardson, D. R., Lane, D. J., Becker, E. M., Huang, M. L., Whitnall, M., Suryo Rahmanto, Y., Sheftel, A. D., and Ponka, P. (2010) Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proc. Natl. Acad. Sci. U.S.A. 107, 10775-10782
18. Dallman, P. R. (1986) Biochemical basis for the manifestations of iron deficiency. Annu. Rev. Nutr. 6, 13-40
19. Allen, G. F., Toth, R., James, J., and Ganley, I. G. (2013) Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. 14, 1127-1135
20. Schiavi, A., Maglioni, S., Palikaras, K., Shaik, A., Strappazzon, F., Brinkmann, V., Torgovnick, A., Castelein, N., De Henau, S., Braeckman, B. P., Cecconi, F., Tavernarakis, N., and Ventura, N. (2015) Iron starvation-induced mitophagy mediates lifespan extension upon mitochondrial stress in C. elegans. Curr. Biol. 25, 1810-1822
21. Eisenstein, R. S., and Ross, K. L. (2003) Novel roles for iron regulatory proteins in the adaptive response to iron deficiency. J. Nutr. 133, 1510S-1516S
22. Yoon, Y. S., Yoon, D. S., Lim, I. K., Yoon, S. H., Chung, H. Y., Rojo, M., Malka, F., Jou, M. J., Martinou, J. C., and Yoon, G. (2006) Formation of elongated giant mitochondria in DFO-induced cellular senescence: involvement of enhanced fusion process through modulation of Fis1. J. Cell Physiol. 209, 468-480
23. Rensvold, J. W., Ong, S. E., Jeevananthan, A., Carr, S. A., Mootha, V. K., and Pagliarini, D. J. (2013) Complementary RNA and protein profiling identifies iron as a key regulator of mitochondrial biogenesis. Cell Rep. 3, 237-245
24. Kaplan, C. D., and Kaplan, J. (2009) Iron acquisition and transcriptional regulation. Chem. Rev. 109, 4536-4552
25. Fan, J., Krautkramer, K. A., Feldman, J. L., and Denu, J. M. (2015) Metabolic regulation of histone post-translational modifications. ACS Chem. Biol. 10, 95-108
26. Gut, P., and Verdin, E. (2013) The nexus of chromatin regulation and intermediary metabolism. Nature 502, 489-498
27. Kaelin, W. G., Jr., and McKnight, S. L. (2013) Influence of metabolism on epigenetics and disease. Cell 153, 56-69
28. McLean, E., Cogswell, M., Egli, I., Wojdyla, D., and de Benoist, B. (2009) Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr. 12, 444-454
29. Shechter, D., Dormann, H. L., Allis, C. D., and Hake, S. B. (2007) Extraction, purification and analysis of histones. Nat. Protoc. 2, 1445-1457
30. Krautkramer, K. A., Reiter, L., Denu, J. M., and Dowell, J. A. (2015) Quantification of SAHA-dependent changes in histone modifications using data-independent acquisition mass spectrometry. J. Proteome Res. 14, 3252-3262
31. Jao, C. Y., and Salic, A. (2008) Exploring RNA transcription and turnover in vivo by using click chemistry. Proc. Natl. Acad. Sci. U.S.A. 105, 15779-15784
32. Ponka, P., and Lok, C. N. (1999) The transferrin receptor: role in health and disease. Int. J. Biochem. Cell Biol. 31, 1111-1137
33. Yao, M., Wang, X., Tang, Y., Zhang, W., Cui, B., Liu, Q., and Xing, L. (2014) Dicer mediating the expression of miR-143 and miR-155 regulates hexokinase II associated cellular response to hypoxia. Am. J. Physiol. Lung Cell Mol. Physiol. 307, L829-L837
34. Burkhart, R. A., Pineda, D. M., Chand, S. N., Romeo, C., Londin, E. R., Karoly, E. D., Cozzitorto, J. A., Rigoutsos, I., Yeo, C. J., Brody, J. R., and Winter, J. M. (2013) HuR is a post-transcriptional regulator of core metabolic enzymes in pancreatic cancer. RNA Biol. 10, 1312-1323
35. Gorospe, M., Tominaga, K., Wu, X., Fähling, M., and Ivan, M. (2011) Post-transcriptional control of the hypoxic response by RNA-binding proteins and microRNAs. Front. Mol. Neurosci. 4, 7
36. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
37. Lok, C. N., and Ponka, P. (1999) Identification of a hypoxia response element in the transferrin receptor gene. J. Biol. Chem. 274, 24147-24152
38. Schofield, C. J., and Ratcliffe, P. J. (2004) Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354
39. Anderson, C. P., Shen, M., Eisenstein, R. S., and Leibold, E. A. (2012) Mammalian iron metabolism and its control by iron regulatory proteins. Biochim. Biophys. Acta 1823, 1468-1483
40. Cloos, P. A., Christensen, J., Agger, K., and Helin, K. (2008) Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 22, 1115-1140
41. Chervona, Y., and Costa, M. (2012) The control of histone methylation and gene expression by oxidative stress, hypoxia, and metals. Free Radic. Biol. Med. 53, 1041-1047
42. McCann, J. C., and Ames, B. N. (2007) An overview of evidence for a causal relation between iron deficiency during development and deficits in cognitive or behavioral function. Am. J. Clin. Nutr. 85, 931-945
43. Fretham, S. J., Carlson, E. S., and Georgieff, M. K. (2011) The role of iron in learning and memory. Adv. Nutr. 2, 112-121
44. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705
45. Berger, S. L. (2007) The complex language of chromatin regulation during transcription. Nature 447, 407-412
46. Zhou, V. W., Goren, A., and Bernstein, B. E. (2011) Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12, 7-18
47. Hamada, S., Kim, T. D., Suzuki, T., Itoh, Y., Tsumoto, H., Nakagawa, H., Janknecht, R., and Miyata, N. (2009) Synthesis and activity of N-oxalylglycine and its derivatives as Jumonji C-domain-containing histone lysine demethylase inhibitors. Bioorg. Med. Chem. Lett. 19, 2852-2855
48. Smith, B. C., and Denu, J. M. (2009) Chemical mechanisms of histone lysine and arginine modifications. Biochim. Biophys. Acta 1789, 45-57
49. Marks, P. A., and Breslow, R. (2007) Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat. Biotechnol. 25, 84-90
50. Finnin, M. S., Donigian, J. R., Cohen, A., Richon, V. M., Rifkind, R. A., Marks, P. A., Breslow, R., and Pavletich, N. P. (1999) Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401, 188-193
51. Netz, D. J., Mascarenhas, J., Stehling, O., Pierik, A. J., and Lill, R. (2014) Maturation of cytosolic and nuclear iron-sulfur proteins. Trends Cell Biol. 24, 303-312
52. Torti, S. V., and Torti, F. M. (2013) Iron and cancer: more ore to be mined. Nat. Rev. Cancer 13, 342-355
53. Rouault, T. A. (2013) Iron metabolism in the CNS: implications for neurodegenerative diseases. Nat. Rev. Neurosci. 14, 551-564
54. Ganz, T., and Nemeth, E. (2015) Iron homeostasis in host defence and inflammation. Nat. Rev. Immunol. 15, 500-510
55. von Haehling, S., Jankowska, E. A., van Veldhuisen, D. J., Ponikowski, P., and Anker, S. D. (2015) Iron deficiency and cardiovascular disease. Nat. Rev. Cardiol. 12, 659-669
56. Xu, W., Barrientos, T., Mao, L., Rockman, H. A., Sauve, A. A., and Andrews, N. C. (2015) Lethal cardiomyopathy in mice lacking transferrin receptor in the heart. Cell Rep. 13, 533-545
57. Galy, B., Ferring-Appel, D., Sauer, S. W., Kaden, S., Lyoumi, S., Puy, H., Kölker, S., Gröne, H. J., and Hentze, M. W. (2010) Iron regulatory proteins secure mitochondrial iron sufficiency and function. Cell Metab. 12, 194-201
58. Barrientos, T., Laothamatas, I., Koves, T. R., Soderblom, E. J., Bryan, M., Moseley, M. A., Muoio, D. M., and Andrews, N. C. (2015) Metabolic catastrophe in mice lacking transferrin receptor in muscle. eBioMedicine 2, 1705-1717
59. Matak, P., Matak, A., Moustafa, S., Aryal, D. K., Benner, E. J., Wetsel, W., and Andrews, N. C. (2016) Disrupted iron homeostasis causes dopaminergic neurodegeneration in mice. Proc. Natl. Acad. Sci. U.S.A. 113, 3428-3435
60. Puccio, H., Simon, D., Cossée, M., Criqui-Filipe, P., Tiziano, F., Melki, J., Hindelang, C., Matyas, R., Rustin, P., and Koenig, M. (2001) Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 27, 181-186
61. Martínez-Reyes, I., Diebold, L. P., Kong, H., Schieber, M., Huang, H., Hensley, C. T., Mehta, M. M., Wang, T., Santos, J. H., Woychik, R., Dufour, E., Spelbrink, J. N., Weinberg, S. E., Zhao, Y., DeBerardinis, R. J., and Chandel, N. S. (2016) TCA cycle and mitochondrial membrane potential are necessary for diverse biological functions. Mol. Cell 61, 199-209
62. Mohrin, M., Shin, J., Liu, Y., Brown, K., Luo, H., Xi, Y., Haynes, C. M., and Chen, D. (2015) Stem cell aging: a mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science 347, 1374-1377