The complex crosstalk between mitochondria and the nucleus: What goes in between?

International Journal of Biochemistry and Cell Biology

Volumn 63, Issue , 2015, Pages 10-15

  Cagin, Umut ^a   Enriquez, José Antonio ^a,b  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

Mitochondria; Mitochondrial capacity; Mitochondrial diseases; Oxidative phosphorylation; Retrograde signaling

Indexed keywords

REACTIVE OXYGEN METABOLITE;

CELL NUCLEUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENERGY METABOLISM; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; PATHOLOGY; SIGNAL TRANSDUCTION;

CELL NUCLEUS; ENERGY METABOLISM; GENE EXPRESSION; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; OXIDATIVE PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84929194905     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2015.01.026     Document Type: Short Survey

References (95)

1. G. Amuthan, G. Biswas, H.K. Ananadatheerthavarada, C. Vijayasarathy, H.M. Shephard, and N.G. Avadhani Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells Oncogene 21 2002 7839 7849
2. G. Amuthan, G. Biswas, S.Y. Zhang, A. Klein-Szanto, C. Vijayasarathy, and N.G. Avadhani Mitochondria-to-nucleus stress signaling induces phenotypic changes, tumor progression and cell invasion EMBO J 20 2001 1910 1920
3. J.J. Arnold, E.D. Smidansky, I.M. Moustafa, and C.E. Cameron Human mitochondrial RNA polymerase: structure-function, mechanism and inhibition Biochim Biophys Acta 1819 2012 948 960
4. T. Arnould, S. Vankoningsloo, P. Renard, A. Houbion, N. Ninane, and C. Demazy CREB activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation EMBO J 21 2002 53 63
5. A. Basu, N. Lenka, J. Mullick, and N.G. Avadhani Regulation of murine cytochrome oxidase Vb gene expression in different tissues and during myogenesis. Role of a YY-1 factor-binding negative enhancer J Biol Chem 272 1997 5899 5908
6. G. Benard, T. Trian, N. Bellance, P. Berger, J. Lavie, and C. Espil-Taris Adaptative capacity of mitochondrial biogenesis and of mitochondrial dynamics in response to pathogenic respiratory chain dysfunction Antioxid Redox Signal 19 2013 350 365
7. 2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk EMBO J 18 1999 522 533
8. G. Biswas, H.K. Anandatheerthavarada, M. Zaidi, and N.G. Avadhani Mitochondria to nucleus stress signaling: a distinctive mechanism of NFkappaB/Rel activation through calcineurin-mediated inactivation of IkappaBbeta J Cell Biol 161 2003 507 519
9. A. Breitkreutz, H. Choi, J.R. Sharom, L. Boucher, V. Neduva, and B. Larsen A global protein kinase and phosphatase interaction network in yeast Science 328 2010 1043 1046
10. R.A. Butow, and N.G. Avadhani Mitochondrial signaling: the retrograde response Mol Cell 14 2004 1 15
11. R.A. Butow, R. Docherty, and V.S. Parikh A path from mitochondria to the yeast nucleus Philos Trans R Soc Lond B: Biol Sci 319 1988 127 133
12. C. Canto, and J. Auwerx PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure Curr Opin Lipidol 20 2009 98 105
13. R. Cerutti, E. Pirinen, C. Lamperti, S. Marchet, A.A. Sauve, and W. Li NAD(+)-dependent activation of Sirt1 corrects the phenotype in a mouse model of mitochondrial disease Cell Metab 19 2014 1042 1049
14. D.C. Chan Fusion and fission: interlinked processes critical for mitochondrial health Annu Rev Genet 46 2012 265 287
15. J.M. Copeland, J. Cho, T. Lo Jr., J.H. Hur, S. Bahadorani, and T. Arabyan Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain Curr Biol: CB 19 2009 1591 1598
16. D. Cristina, M. Cary, A. Lunceford, C. Clarke, and C. Kenyon A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans PLoS Genet 5 2009 e1000450
17. J.T. Cunningham, J.T. Rodgers, D.H. Arlow, F. Vazquez, V.K. Mootha, and P. Puigserver mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex Nature 450 2007 736 740
18. R. Delsite, S. Kachhap, R. Anbazhagan, E. Gabrielson, and K.K. Singh Nuclear genes involved in mitochondria-to-nucleus communication in breast cancer cells Mol Cancer 1 2002 6
19. I. Dilova, S. Aronova, J.C. Chen, and T. Powers Tor signaling and nutrient-based signals converge on Mks1p phosphorylation to regulate expression of Rtg1.Rtg3p-dependent target genes J Biol Chem 279 2004 46527 46535
20. I. Dilova, C.Y. Chen, and T. Powers Mks1 in concert with TOR signaling negatively regulates RTG target gene expression in S. cerevisiae Curr Biol: CB 12 2002 389 395
21. J. Durieux, S. Wolff, and A. Dillin The cell-non-autonomous nature of electron transport chain-mediated longevity Cell 144 2011 79 91
22. J.A. Enriquez, P. Fernandez-Silva, and J. Montoya Autonomous regulation in mammalian mitochondrial DNA transcription Biol Chem 380 1999 737 747
23. C.B. Epstein, J.A. Waddle, V. Hale Wt Dave, J. Thornton, and T.L. Macatee Genome-wide responses to mitochondrial dysfunction Mol Biol Cell 12 2001 297 308
24. L. Ernster, D. Ikkos, and R. Luft Enzymic activities of human skeletal muscle mitochondria: a tool in clinical metabolic research Nature 184 1959 1851 1854
25. M. Fan, J. Rhee, J. St-Pierre, C. Handschin, P. Puigserver, and J. Lin Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1alpha: modulation by p38 MAPK Genes Dev 18 2004 278 289
26. W.A. Freije, S. Mandal, and U. Banerjee Expression profiling of attenuated mitochondrial function identifies retrograde signals in Drosophila G3 2 2012 843 851
27. G. Gasparre, G. Romeo, M. Rugolo, and A.M. Porcelli Learning from oncocytic tumors: why choose inefficient mitochondria Biochim Biophys Acta 1807 2011 633 642
28. D. Ghezzi, and M. Zeviani Assembly factors of human mitochondrial respiratory chain complexes: physiology and pathophysiology Adv Exp Med Biol 748 2012 65 106
29. S. Giannattasio, Z. Liu, J. Thornton, and R.A. Butow Retrograde response to mitochondrial dysfunction is separable from TOR1/2 regulation of retrograde gene expression J Biol Chem 280 2005 42528 42535
30. N. Gleyzer, and R.C. Scarpulla PGC-1-related coactivator (PRC), a sensor of metabolic stress, orchestrates a redox-sensitive program of inflammatory gene expression J Biol Chem 286 2011 39715 39725
31. N. Gleyzer, and R.C. Scarpulla Activation of a PGC-1-related coactivator (PRC)-dependent inflammatory stress program linked to apoptosis and premature senescence J Biol Chem 288 2013 8004 8015
32. M. Guha, S. Srinivasan, G. Biswas, and N.G. Avadhani Activation of a novel calcineurin-mediated insulin-like growth factor-1 receptor pathway, altered metabolism, and tumor cell invasion in cells subjected to mitochondrial respiratory stress J Biol Chem 282 2007 14536 14546
33. C.M. Haynes, and D. Ron The mitochondrial UPR-protecting organelle protein homeostasis J Cell Sci 123 2010 3849 3855
34. A. Heddi, P. Lestienne, D.C. Wallace, and G. Stepien Mitochondrial DNA expression in mitochondrial myopathies and coordinated expression of nuclear genes involved in ATP production J Biol Chem 268 1993 12156 12163
35. T. Horibe, and N.J. Hoogenraad The chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response PLoS ONE 2 2007 e835
36. R.H. Houtkooper, L. Mouchiroud, D. Ryu, N. Moullan, E. Katsyuba, and G. Knott Mitonuclear protein imbalance as a conserved longevity mechanism Nature 497 2013 451 457
37. K. Ishikawa, O. Hashizume, N. Koshikawa, S. Fukuda, K. Nakada, and K. Takenaga Enhanced glycolysis induced by mtDNA mutations does not regulate metastasis FEBS Lett 582 2008 3525 3530
38. R.S. Jahangir Tafrechi, P.J. Svensson, G.M. Janssen, K. Szuhai, J.A. Maassen, and A.K. Raap Distinct nuclear gene expression profiles in cells with mtDNA depletion and homoplasmic A3243G mutation Mutat Res 578 2005 43 52
39. S.M. Jazwinski The retrograde response: when mitochondrial quality control is not enough Biochim Biophys Acta 1833 2013 400 409
40. Y. Jia, B. Rothermel, J. Thornton, and R.A. Butow A basic helix-loop-helix-leucine zipper transcription complex in yeast functions in a signaling pathway from mitochondria to the nucleus Mol Cell Biol 17 1997 1110 1117
41. A.W. Jones, Z. Yao, J.M. Vicencio, A. Karkucinska-Wieckowska, and G. Szabadkai PGC-1 family coactivators and cell fate: roles in cancer, neurodegeneration, cardiovascular disease and retrograde mitochondria-nucleus signalling Mitochondrion 12 2012 86 99
42. S. Kawai, J. Urban, M. Piccolis, N. Panchaud, C. De Virgilio, and R. Loewith Mitochondrial genomic dysfunction causes dephosphorylation of Sch9 in the yeast Saccharomyces cerevisiae Eukaryot Cell 10 2011 1367 1369
43. N.A. Khan, M. Auranen, I. Paetau, E. Pirinen, L. Euro, and S. Forsstrom Effective treatment of mitochondrial myopathy by nicotinamide riboside, a vitamin B3 EMBO Mol Med 6 2014 721 731
44. P.A. Kirchman, S. Kim, C.Y. Lai, and S.M. Jazwinski Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae Genetics 152 1999 179 190
45. A. Komeili, K.P. Wedaman, E.K. O'Shea, and T. Powers Mechanism of metabolic control. Target of rapamycin signaling links nitrogen quality to the activity of the Rtg1 and Rtg3 transcription factors J Cell Biol 151 2000 863 878
46. M. Kulawiec, K.M. Owens, and K.K. Singh Cancer cell mitochondria confer apoptosis resistance and promote metastasis Cancer Biol Ther 8 2009 1378 1385
47. M. Laplante, and D.M. Sabatini mTOR signaling in growth control and disease Cell 149 2012 274 293
48. E. Lapuente-Brun, R. Moreno-Loshuertos, R. Acin-Perez, A. Latorre-Pellicer, C. Colas, and E. Balsa Supercomplex assembly determines electron flux in the mitochondrial electron transport chain Science 340 2013 1567 1570
49. S.J. Lee, A.B. Hwang, and C. Kenyon Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity Curr Biol: CB 20 2010 2131 2136
50. X.S. Liao, W.C. Small, P.A. Srere, and R.A. Butow Intramitochondrial functions regulate nonmitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae Mol Cell Biol 11 1991 38 46
51. J. Lin, C. Handschin, and B.M. Spiegelman Metabolic control through the PGC-1 family of transcription coactivators Cell Metab 1 2005 361 370
52. M.T. Lin, D.K. Simon, C.H. Ahn, L.M. Kim, and M.F. Beal High aggregate burden of somatic mtDNA point mutations in aging and Alzheimer's disease brain Hum Mol Genet 11 2002 133 145
53. J. Liu, Q. Wu, D. He, T. Ma, L. Du, and W. Dui Drosophila sbo regulates lifespan through its function in the synthesis of coenzyme Q in vivo J Genet Genomics Yi chuan xue bao 38 2011 225 234
54. Z. Liu, and R.A. Butow Mitochondrial retrograde signaling Annu Rev Genet 40 2006 159 185
55. A.F. MacAskill, and J.T. Kittler Control of mitochondrial transport and localization in neurons Trends Cell Biol 20 2010 102 112
56. R.D. Martinus, G.P. Garth, T.L. Webster, P. Cartwright, D.J. Naylor, and P.B. Hoj Selective induction of mitochondrial chaperones in response to loss of the mitochondrial genome Eur J Biochem 240 1996 98 103 FEBS
57. M.F. Marusich, B.H. Robinson, J.W. Taanman, S.J. Kim, R. Schillace, and J.L. Smith Expression of mtDNA and nDNA encoded respiratory chain proteins in chemically and genetically-derived Rho0 human fibroblasts: a comparison of subunit proteins in normal fibroblasts treated with ethidium bromide and fibroblasts from a patient with mtDNA depletion syndrome Biochim Biophys Acta 1362 1997 145 159
58. M.T. McCammon, C.B. Epstein, B. Przybyla-Zawislak, L. McAlister-Henn, and R.A. Butow Global transcription analysis of Krebs tricarboxylic acid cycle mutants reveals an alternating pattern of gene expression and effects on hypoxic and oxidative genes Mol Biol Cell 14 2003 958 972
59. M. McKenzie, E.J. Tucker, A.G. Compton, M. Lazarou, C. George, and D.R. Thorburn Mutations in the gene encoding C8orf38 block complex I assembly by inhibiting production of the mitochondria-encoded subunit ND1 J Mol Biol 414 2011 413 426
60. M.V. Miceli, and S.M. Jazwinski Nuclear gene expression changes due to mitochondrial dysfunction in ARPE-19 cells: implications for age-related macular degeneration Investig Ophthalmol Vis Sci 46 2005 1765 1773
61. D.U. Mick, M. Vukotic, H. Piechura, H.E. Meyer, B. Warscheid, and M. Deckers Coa3 and Cox14 are essential for negative feedback regulation of COX1 translation in mitochondria J Cell Biol 191 2010 141 154
62. R. Mineri, N. Pavelka, E. Fernandez-Vizarra, P. Ricciardi-Castagnoli, M. Zeviani, and V. Tiranti How do human cells react to the absence of mitochondrial DNA? PLoS ONE 4 2009 e5713
63. A. Mottis, V. Jovaisaite, and J. Auwerx The mitochondrial unfolded protein response in mammalian physiology Mamm Genome: Off J Int Mamm Genome Soc 25 2014 424 433
64. V.S. Parikh, M.M. Morgan, R. Scott, L.S. Clements, and R.A. Butow The mitochondrial genotype can influence nuclear gene expression in yeast Science 235 1987 576 580
65. S. Peralta, X. Wang, and C.T. Moraes Mitochondrial transcription: lessons from mouse models Biochim Biophys Acta 1819 2012 961 969
66. G. Pfeffer, K. Majamaa, D.M. Turnbull, D. Thorburn, and P.F. Chinnery Treatment for mitochondrial disorders Cochrane Database Syst Rev 4 2012 CD004426
67. E. Pirinen, C. Canto, Y.S. Jo, L. Morato, H. Zhang, and K.J. Menzies Pharmacological Inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle Cell Metab 19 2014 1034 1041
68. P.E. Porporato, V.L. Payen, J. Perez-Escuredo, C.J. De Saedeleer, P. Danhier, and T. Copetti A mitochondrial switch promotes tumor metastasis Cell Rep 8 2014 754 766
69. R.O. Poyton, and J.E. McEwen Crosstalk between nuclear and mitochondrial genomes Annu Rev Biochem 65 1996 563 607
70. A.K. Reeve, K.J. Krishnan, and D.M. Turnbull Age related mitochondrial degenerative disorders in humans Biotechnol J 3 2008 750 756
71. J. Rorbach, and M. Minczuk The post-transcriptional life of mammalian mitochondrial RNA Biochem J 444 2012 357 373
72. B.A. Rothermel, J.L. Thornton, and R.A. Butow Rtg3p, a basic helix-loop-helix/leucine zipper protein that functions in mitochondrial-induced changes in gene expression, contains independent activation domains J Biol Chem 272 1997 19801 19807
73. E.I. Rugarli, and T. Langer Mitochondrial quality control: a matter of life and death for neurons EMBO J 31 2012 1336 1349
74. E. Sahin, S. Colla, M. Liesa, J. Moslehi, F.L. Muller, and M. Guo Telomere dysfunction induces metabolic and mitochondrial compromise Nature 470 2011 359 365
75. R.C. Scarpulla Nuclear control of respiratory gene expression in mammalian cells J Cell Biochem 97 2006 673 683
76. R.C. Scarpulla Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator Ann N Y Acad Sci 1147 2008 321 334
77. R.C. Scarpulla Transcriptional paradigms in mammalian mitochondrial biogenesis and function Physiol Rev 88 2008 611 638
78. R.C. Scarpulla Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network Biochim Biophys Acta 1813 2011 1269 1278
79. R.C. Scarpulla Nucleus-encoded regulators of mitochondrial function: integration of respiratory chain expression, nutrient sensing and metabolic stress Biochim Biophys Acta 1819 2012 1088 1097
80. S.N. Schreiber, R. Emter, M.B. Hock, D. Knutti, J. Cardenas, and M. Podvinec The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis Proc Natl Acad Sci USA 101 2004 6472 6477
81. T. Sekito, J. Thornton, and R.A. Butow Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p Mol Biol Cell 11 2000 2103 2115
82. D.K. Simon, M.T. Lin, L. Zheng, G.J. Liu, C.H. Ahn, and L.M. Kim Somatic mitochondrial DNA mutations in cortex and substantia nigra in aging and Parkinson's disease Neurobiol Aging 25 2004 71 81
83. V. Srinivasan, A. Kriete, A. Sacan, and S.M. Jazwinski Comparing the yeast retrograde response and NF-kappaB stress responses: implications for aging Aging Cell 9 2010 933 941
84. R.H. Swerdlow The neurodegenerative mitochondriopathies J Alzheimers Dis: JAD 17 2009 737 751
85. A. Traven, J.M. Wong, D. Xu, M. Sopta, and C.J. Ingles Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial DNA mutant J Biol Chem 276 2001 4020 4027
86. S.B. Vafai, and V.K. Mootha Mitochondrial disorders as windows into an ancient organelle Nature 491 2012 374 383
87. J.R. Vanfleteren, and A. De Vreese The gerontogenes age-1 and daf-2 determine metabolic rate potential in aging Caenorhabditis elegans FASEB J: Off Publ Fed Am Soc Exp Biol 9 1995 1355 1361
88. K. Vercauteren, R.A. Pasko, N. Gleyzer, V.M. Marino, and R.C. Scarpulla PGC-1-related coactivator: immediate early expression and characterization of a CREB/NRF-1 binding domain associated with cytochrome c promoter occupancy and respiratory growth Mol Cell Biol 26 2006 7409 7419
89. 2+ homeostasis in respiratory chain-deficient cells but efficient compensation of energetic disadvantage by enhanced anaerobic glycolysis due to low ATP steady state levels Exp Cell Res 313 2007 3076 3089
90. H. Wang, and R. Morais Up-regulation of nuclear genes in response to inhibition of mitochondrial DNA expression in chicken cells Biochim Biophys Acta 1352 1997 325 334
91. J. Wang, J.C. Jiang, and S.M. Jazwinski Gene regulatory changes in yeast during life extension by nutrient limitation Exp Gerontol 45 2010 621 631
92. T. Wenz Mitochondria and PGC-1alpha in aging and age-associated diseases J Aging Res 2011 2011 810619
93. T. Wenz Regulation of mitochondrial biogenesis and PGC-1alpha under cellular stress Mitochondrion 13 2013 134 142
94. R.J. Youle, and D.P. Narendra Mechanisms of mitophagy Nat Rev Mol Cell Biol 12 2011 9 14
95. Z. Zhang, Z. Hailat, M.J. Falk, and X.W. Chen Integrative analysis of independent transcriptome data for rare diseases Methods 69 2014 315 325