Mitochondrial signaling: Forwards, backwards, and in between

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Whelan, Sean P ^a   Zuckerbraun, Brian S ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR SIGNALING; ENERGY PRODUCTIONS; EUKARYOTIC CELLS; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL FUNCTION; NUCLEAR GENE EXPRESSION; STRESS RESPONSE; UNFOLDED PROTEIN RESPONSE;

SIGNALING; TRANSCRIPTION FACTORS;

MITOCHONDRIA;

ACTIVATING TRANSCRIPTION FACTOR 2; CALCINEURIN; CELL NUCLEUS DNA; CHAPERONIN 60; CITRATE SYNTHASE; CYTOCHROME C; DOUBLE STRANDED DNA; ESTROGEN RELATED RECEPTOR ALPHA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN 70; MITOCHONDRIAL DNA; MITOCHONDRIAL RNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; REACTIVE OXYGEN METABOLITE; RNA POLYMERASE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR SP1;

AEROBIC METABOLISM; AUTOPHAGY; BIOGENESIS; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL STRUCTURE; CELLULAR STRESS RESPONSE; EUKARYOTIC CELL; FATTY ACID OXIDATION; GENE EXPRESSION; GLYCOLYSIS; HUMAN; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LONGEVITY; MAMMAL CELL; MICROARRAY ANALYSIS; MITOCHONDRIAL GENOME; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHAGOSOME; REVIEW; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOLOGICAL MODEL; CELL NUCLEUS; METABOLISM; PHYSIOLOGICAL STRESS; SIGNAL TRANSDUCTION;

EUKARYOTA;

ANIMALS; CELL NUCLEUS; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84879356734     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/351613     Document Type: Review

References (85)

1. Ernster L., Schatz G., Mitochondria: a historical review. Journal of Cell Biology 1981 91 3, part 2 227s 255s 2-s2.0-0019835356
2. Scarpulla R. C., Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiological Reviews 2008 88 2 611 638 2-s2.0-42049114034 10.1152/physrev.00025.2007
3. Parikh V. S., Morgan M. M., Scott R., Clements L. S., Butow R. A., The mitochondrial genotype can influence nuclear gene expression in yeast. Science 1987 235 4788 576 580 2-s2.0-0023106633
4. Pejznochova M., Tesarova M., Hansikova H., Magner M., Honzik T., Vinsova K., Hajkova Z., Havlickova V., Zeman J., Mitochondrial DNA content and expression of genes involved in mtDNA transcription, regulation and maintenance during human fetal development. Mitochondrion 2010 10 4 321 329 2-s2.0-77952885904 10.1016/j.mito.2010.01.006
5. Hsieh C. J., Weng S. W., Liou C. W., Lin T. K., Chen J. B., Tiao M. M., Hung Y. T., Chen I. Y., Huang W. T., Wang P. W., Tissue-specific differences in mitochondrial DNA content in type 2 diabetes. Diabetes Research and Clinical Practice 2011 92 1 106 110 2-s2.0-79954578362 10.1016/j.diabres.2011.01.010
6. Wallace D. C., Mitochondria, bioenergetics, and the epigenome in eukaryotic and human evolution. Cold Spring Harbor Symposia on Quantitative Biology 2009 74 383 393 2-s2.0-77957730674 10.1101/sqb.2009.74.031
7. Scarpulla R. C., Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochimica et Biophysica Acta 2002 1576 1-2 1 14 2-s2.0-0037036115 10.1016/S0167-4781(02)00343-3
8. Fisher R. P., Clayton D. A., A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy- and light-strand promoters dissected and reconstituted in vitro. The Journal of Biological Chemistry 1985 260 20 11330 11338 2-s2.0-0022212873
9. Fisher R. P., Clayton D. A., Purification and characterization of human mitochondrial transcription factor 1. Molecular and Cellular Biology 1988 8 8 3496 3509 2-s2.0-0023684801
10. Amiott E. A., Jaehning J. A., Mitochondrial transcription is regulated via an ATP "sensing" mechanism that couples RNA abundance to respiration. Molecular Cell 2006 22 3 329 338 2-s2.0-33646163885 10.1016/j.molcel.2006.03.031
11. Tracy R. L., Stern D. B., Mitochondrial transcription initiation: promotor structures and RNA polymerases. Current Genetics 1995 28 3 205 216 2-s2.0-0029116754 10.1007/BF00309779
12. Tiranti V., Savoia A., Forti F., D'Apolito M. F., Centra M., Rocchi M., Zeviani M., Identification of the gene encoding the human mitochondrial RNA polymerase (h-mtRPOL) by cyberscreening of the expressed sequence tags database. Human Molecular Genetics 1997 6 4 615 625 2-s2.0-0030943170 10.1093/hmg/6.4.615
13. Evans M. J., Scarpulla R. C., Both upstream and intron sequence elements are required for elevated expression of the rat somatic cytochrome c gene in COS-1 cells. Molecular and Cellular Biology 1988 8 1 35 41 2-s2.0-0023746896
14. Evans M. J., Scarpulla R. C., Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. The Journal of Biological Chemistry 1989 264 24 14361 14368 2-s2.0-0024358781
15. Scarpulla R. C., Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 2002 286 1 81 89 2-s2.0-0037029049 10.1016/S0378-1119(01)00809-5
16. Evans M. J., Scarpulla R. C., NRF-1: a trans-activator of nuclear-encoded respiratory genes in animal cells. Genes and Development 1990 4 6 1023 1034 2-s2.0-0025313512
17. Zaid A., Li R., Luciakova K., Barath P., Nery S., Nelson B. D., On the role of the general transcription factor Sp1 in the activation and repression of diverse mammalian oxidative phosphorylation genes. Journal of Bioenergetics and Biomembranes 1999 31 2 129 135 2-s2.0-0032780688 10.1023/A:1005499727732
18. Spiegelman B. M., Transcriptional control of energy homeostasis through the PGC1 coactivators. Novartis Foundation Symposium 2007 286 196 203 2-s2.0-42449132297
19. Meirhaeghe A., Crowley V., Lenaghan C., Lelliott C., Green K., Stewart A., Hart K., Schinner S., Sethi J. K., Yeo G., Brand M. D., Cortright R. N., O'Rahilly S., Montague C., Vidal-Puig A. J., Characterization of the human, mouse and rat PGC1 β (peroxisomeproliferator-activated receptor- γ co-activator 1 β) gene in vitro and in vivo. Biochemical Journal 2003 373 1 155 165 2-s2.0-0038682372 10.1042/BJ20030200
20. 2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk. EMBO Journal 1999 18 3 522 533 2-s2.0-0033081478 10.1093/emboj/18.3.522
21. Schwarzlander M., Konig A. C., Sweetlove L. J., Finkemeier I., The impact of impaired mitochondrial function on retrograde signalling: a meta-analysis of transcriptomic responses. Journal of Experimental Botany 2012 4 1735 1750
22. Liao X., Small W. C., Srere P. A., Butow R. A., Intramitochondrial functions regulate nonmitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae. Molecular and Cellular Biology 1991 11 1 38 46 2-s2.0-0026085418
23. Liao X., Butow R. A., RTG1 and RTG2: two yeast genes required for a novel path of communication from mitochondria to the nucleus. Cell 1993 72 1 61 71 2-s2.0-0027524176 10.1016/0092-8674(93)90050-Z
24. Liu Z., Butow R. A., A transcriptional switch in the expression of yeast tricarboxylic acid cycle genes in response to a reduction or loss of respiratory function. Molecular and Cellular Biology 1999 19 10 6720 6728 2-s2.0-0032873464
25. Epstein C. B., Waddle J. A., Hale W., Davé V., Thornton J., Macatee T. L., Garner H. R., Butow R. A., Genome-wide responses to mitochondrial dysfunction. Molecular Biology of the Cell 2001 12 2 297 308 2-s2.0-0035157544
26. Freije W. A., Mandal S., Banerjee U., Expression profiling of attenuated mitochondrial function identifies retrograde signals in Drosophila. G3 2012 2 8 843 851 10.1534/g3.112.002584
27. Liu Z., Spírek M., Thornton J., Butow R. A., A novel degron-mediated degradation of the RTG pathway regulator, Mks1p, by SCF. Molecular Biology of the Cell 2005 16 10 4893 4904 2-s2.0-26244451589 10.1091/mbc.E05-06-0516
28. Liu Z., Butow R. A., Mitochondrial retrograde signaling. Annual Review of Genetics 2006 40 159 185 2-s2.0-33845656956 10.1146/annurev.genet.40.110405. 090613
29. Dilova I., Chen C. Y., Powers T., Mks1 in concert with TOR signaling negatively regulates RTG target gene expression in S. cerevisiae. Current Biology 2002 12 5 389 395 2-s2.0-0037022532 10.1016/S0960-9822(02)00677-2
30. Liu Z., Sekito T., Špírek M., Thornton J., Butow R. A., Retrograde signaling is regulated by the dynamic interaction between Rtg2p and Mks1p. Molecular Cell 2003 12 2 401 411 2-s2.0-0141922982 10.1016/S1097-2765(03) 00285-5
31. Owusu-Ansah E., Yavari A., Mandal S., Banerjee U., Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nature Genetics 2008 40 3 356 361 2-s2.0-39749104169 10.1038/ng.2007.50
32. Berridge M. J., Bootman M. D., Lipp P., Calcium-a life and death signal. Nature 1998 395 6703 645 648 2-s2.0-0032531818 10.1038/27094
33. Carafoli E., The interplay of mitochondria with calcium: an historical appraisal. Cell Calcium 2012 52 1 1 8 10.1016/j.ceca.2012.02.007
34. Nicholls D. G., Mitochondria and calcium signaling. Cell Calcium 2005 38 3-4 311 317 2-s2.0-24644462789 10.1016/j.ceca.2005.06.011
35. Bayir H., Kagan V. E., Bench-to-bedside review: mitochondrial injury, oxidative stress and apoptosis-there is nothing more practical than a good theory. Critical Care 2008 12 1, article 206 2-s2.0-45549094799 10.1186/cc6779
36. Butow R. A., Avadhani N. G., Mitochondrial signaling: the retrograde response. Molecular Cell 2004 14 1 1 15 2-s2.0-1842665662 10.1016/S1097-2765(04) 00179-0
37. Amuthan G., Biswas G., Ananadatheerthavarada H. K., Vijayasarathy C., Shephard H. M., Avadhani N. G., Mitochondrial stress-induced calcium signaling, phenotypic changes and invasive behavior in human lung carcinoma A549 cells. Oncogene 2002 21 51 7839 7849 2-s2.0-0037038669 10.1038/sj.onc.1205983
38. Arnould T., Vankoningsloo S., Renard P., Houbion A., Ninane N., Demazy C., Remacle J., Raes M., Creb activation induced by mitochondrial dysfunction is a new signaling pathway that impairs cell proliferation. EMBO Journal 2002 21 1-2 53 63 2-s2.0-0037080987 10.1093/emboj/21.1.53
39. Vankoningsloo S., de Pauw A., Houbion A., Tejerina S., Demazy C., de Longueville F., Bertholet V., Renard P., Remacle J., Holvoet P., Raes M., Arnould T., CREB activation induced by mitochondrial dysfunction triggers triglyceride accumulation in 3T3-L1 preadipocytes. Journal of Cell Science 2006 119 part 7 1266 1282 2-s2.0-33646819645 10.1242/jcs.02848
40. Biswas G., Anandatheerthavarada H. K., Zaidi M., Avadhani N. G., Mitochondria to nucleus stress signaling: a distinctive mechanism of NF B/Rel activation through calcineurin-mediated inactivation of I B β Journal of Cell Biology 2003 161 3 507 519 2-s2.0-0038612839 10.1083/jcb.200211104
41. Srinivasan V., Kriete A., Sacan A., Jazwinski S. M., Comparing the yeast retrograde response and NF- B stress responses: implications for aging. Aging Cell 2010 9 6 933 941 2-s2.0-78249243079 10.1111/j.1474-9726.2010.00622.x
42. Le Bras M., Clément M. V., Pervaiz S., Brenner C., Reactive oxygen species and the mitochondrial signaling pathway of cell death. Histology and Histopathology 2005 20 1 205 219 2-s2.0-11144303507
43. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J. D., Yamamoto M., Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes and Development 1999 13 1 76 86 2-s2.0-0032953192
44. Formentini L., Sanchez-Arago M., Sanchez-Cenizo L., Cuezva J. M., The mitochondrial ATPase inhibitory factor 1 triggers a ROS-mediated retrograde prosurvival and proliferative response. Molecular Cell 2012 45 6 731 742 10.1016/j.molcel.2012.01.008
45. Park J. S., Sharma L. K., Li H., Xiang R., Holstein D., Wu J., Lechleiter J., Naylor S. L., Deng J. J., Lu J., Bai Y., A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Human Molecular Genetics 2009 18 9 1578 1589 2-s2.0-64549098628 10.1093/hmg/ddp069
46. Lee H. C., Chang C. M., Chi C. W., Somatic mutations of mitochondrial DNA in aging and cancer progression. Ageing Research Reviews 2010 9 supplement 1 S47 S58 2-s2.0-77957938682 10.1016/j.arr.2010.08.009
47. Correia R. L., Oba-Shinjo S. M., Uno M., Huang N., Marie S. K. N., Mitochondrial DNA depletion and its correlation with TFAM, TFB1M, TFB2M and POLG in human diffusely infiltrating astrocytomas. Mitochondrion 2011 11 1 48 53 2-s2.0-78650021675 10.1016/j.mito.2010.07.001
48. Wallace D. C., Mitochondria and cancer. Nature Reviews Cancer 2012 12 10 685 698
49. Pellegrino M. W., Nargund A. M., Haynes C. M., Signaling the mitochondrial unfolded protein response. Biochimica et Biophysica Acta 2013 1833 2 410 416 10.1016/j.bbamcr.2012.02.019
50. Haynes C. M., Petrova K., Benedetti C., Yang Y., Ron D., ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Developmental Cell 2007 13 4 467 480 2-s2.0-34848861368 10.1016/j.devcel.2007. 07.016
51. Broadley S. A., Hartl F. U., Mitochondrial stress signaling: a pathway unfolds. Trends in Cell Biology 2008 18 1 1 4 2-s2.0-37849022851 10.1016/j.tcb.2007.11.003
52. Aldridge J. E., Horibe T., Hoogenraad N. J., Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS ONE 2007 2 9, article e874 2-s2.0-37849048003 10.1371/journal.pone.0000874
53. Horibe T., Hoogenraad N. J., The Chop gene contains an element for the positive regulation of the mitochondrial unfolded protein response. PLoS ONE 2007 2 9, article e835 2-s2.0-37849038317 10.1371/journal.pone.0000835
54. Siegelin M. D., Dohi T., Raskett C. M., Orlowski G. M., Powers C. M., Gilbert C. A., Ross A. H., Plescia J., Altieri D. C., Exploiting the mitochondrial unfolded protein response for cancer therapy in mice and human cells. Journal of Clinical Investigation 2011 121 4 1349 1360 2-s2.0-79953317434 10.1172/JCI44855
55. Papa L., Germain D., Estrogen receptor mediates a distinct mitochondrial unfolded protein response. Journal of Cell Science 2011 124 9 1396 1402 2-s2.0-79955549674 10.1242/jcs.078220
56. Bernales S., Soto M. M., McCullagh E., Unfolded protein stress in the endoplasmic reticulum and mitochondria: a role in neurodegeneration. Frontiers in Aging Neuroscience 2012 4 article 5 10.3389/fnagi.2012.00005
57. Witte M. E., Nijland P. G., Drexhage J. A., Reduced expression of PGC-1 partly underlies mitochondrial changes and correlates with neuronal loss in multiple sclerosis cortex. Acta Neuropathologica 2013 125 2, article 231
58. Zorov D. B., Juhaszova M., Sollott S. J., Mitochondrial ROS-induced ROS release: an update and review. Biochimica et Biophysica Acta 2006 1757 5-6 509 517 2-s2.0-33745684904 10.1016/j.bbabio.2006.04.029
59. Zorov D. B., Filburn C. R., Klotz L. O., Zweier J. L., Sollott S. J., Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. Journal of Experimental Medicine 2000 192 7 1001 1014 2-s2.0-0034596947 10.1084/jem.192.7.1001
60. Zhou L., Aon M. A., Almas T., Cortassa S., Winslow R. L., O'Rourke B., A reaction-diffusion model of ROS-induced ROS release in a mitochondrial network. PLoS Computational Biology 2010 6 1 2-s2.0-76749088967 10.1371/journal.pcbi. 1000657 e1000657
61. Park J., Choi C., Contribution of mitochondrial network dynamics to intracellular ROS signaling. Communicative and Integrative Biology 2012 5 1 81 83 10.4161/cib.18257
62. Zinkevich N. S., Gutterman D. D., ROS-induced ROS release in vascular biology: redox-redox signaling. The American Journal of Physiology 2011 301 3 H647 H653
63. Huang J., Lam G. Y., Brumell J. H., Autophagy signaling through reactive oxygen species. Antioxidants and Redox Signaling 2011 14 11 2215 2231 2-s2.0-79956118584 10.1089/ars.2010.3554
64. Kadandale P., Kiger A. A., Role of selective autophagy in cellular remodeling: "self-eating" into shape. Autophagy 2010 6 8 1194 1195 2-s2.0-78649253110 10.4161/auto.6.8.13476
65. Wang Y., Nartiss Y., Steipe B., McQuibban G. A., Kim P. K., ROS-induced mitochondrial depolarization initiates PARK2/PARKIN-dependent mitochondrial degradation by autophagy. Autophagy 2012 8 10 1462 1476
66. Chen X., Li M., Chen D., Gao W., Guan J. L., Komatsu M., Yin X. M., Autophagy induced by calcium phosphate precipitates involves endoplasmic reticulum membranes in autophagosome biogenesis. PLoS ONE 2012 7 12 e52347 10.1371/journal.pone.0052347
67. Arnoult D., Rismanchi N., Grodet A., Roberts R. G., Seeburg D. P., Estaquier J., Sheng M., Blackstone C., Bax/bak-dependent release of DDP/TIMM8a promotes Drp1-mediated mitochondrial fission and mitoptosis during programmed cell death. Current Biology 2005 15 23 2112 2118 2-s2.0-28444487509 10.1016/j.cub.2005.10.041
68. Lyamzaev K. G., Nepryakhina O. K., Saprunova V. B., Bakeeva L. E., Pletjushkina O. Y., Chernyak B. V., Skulachev V. P., Novel mechanism of elimination of malfunctioning mitochondria (mitoptosis): formation of mitoptotic bodies and extrusion of mitochondrial material from the cell. Biochimica et Biophysica Acta 2008 1777 7-8 817 825 2-s2.0-46349099816 10.1016/j.bbabio.2008. 03.027
69. Chen S. D., Yang D. I., Lin T. K., Shaw F. Z., Liou C. W., Chuang Y. C., Roles of oxidative stress, apoptosis, PGC-1 and mitochondrial biogenesis in cerebral ischemia. International Journal of Molecular Sciences 2011 12 10 7199 7215 10.3390/ijms12107199
70. Gleyzer N., Vercauteren K., Scarpulla R. C., Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Molecular and Cellular Biology 2005 25 4 1354 1366 2-s2.0-13444306450 10.1128/MCB.25.4.1354-1366.2005
71. 2+ concentration during the cell cycle and the onset of differentiation in L6E9 myoblasts. The American Journal of Physiology 2009 296 5 C1185 C1194 2-s2.0-66149087262 10.1152/ajpcell.00377.2008
72. Underhill D. M., Ozinsky A., Phagocytosis of microbes: complexity in action. Annual Review of Immunology 2002 20 825 852 2-s2.0-0036216769 10.1146/annurev.immunol.20.103001.114744
73. West A. P., Brodsky I. E., Rahner C., Woo D. K., Erdjument-Bromage H., Tempst P., Walsh M. C., Choi Y., Shadel G. S., Ghosh S., TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 2011 472 7344 476 480 2-s2.0-79955532516 10.1038/nature09973
74. Harman D., Aging: a theory based on free radical and radiation chemistry. Journal of Gerontology 1956 11 3 298 300 2-s2.0-77049308856
75. Barja G., Herrero A., Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB Journal 2000 14 2 312 318 2-s2.0-0033972463
76. Severin F. F., Severina I. I., Antonenko Y. N., Rokitskaya T. I., Cherepanov D. A., Mokhova E. N., Vyssokikh M. Y., Pustovidko A. V., Markova O. V., Yaguzhinsky L. S., Korshunova G. A., Sumbatyan N. V., Skulachev M. V., Skulachev V. P., Penetrating cation/fatty acid anion pair as a mitochondria-targeted protonophore. Proceedings of the National Academy of Sciences of the United States of America 2010 107 2 663 668 2-s2.0-76249108242 10.1073/pnas.0910216107
77. Skulachev V. P., Anisimov V. N., Antonenko Y. N., Bakeeva L. E., Chernyak B. V., Erichev V. P., Filenko O. F., Kalinina N. I., Kapelko V. I., Kolosova N. G., Kopnin B. P., Korshunova G. A., Lichinitser M. R., Obukhova L. A., Pasyukova E. G., Pisarenko O. I., Roginsky V. A., Ruuge E. K., Senin I. I., Severina I. I., Skulachev M. V., Spivak I. M., Tashlitsky V. N., Tkachuk V. A., Vyssokikh M. Y., Yaguzhinsky L. S., Zorov D. B., An attempt to prevent senescence: a mitochondrial approach. Biochimica et Biophysica Acta 2009 1787 5 437 461 2-s2.0-67349283471 10.1016/j.bbabio.2008.12.008
78. Smith R. A., Porteous C. M., Coulter C. V., Murphy M. P., Selective targeting of an antioxidant to mitochondria. European Journal of Biochemistry 1999 263 3 709 716 10.1046/j.1432-1327.1999.00543.x
79. James A. M., Cochemé H. M., Smith R. A. J., Murphy M. P., Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species: implications for the use of exogenous ubiquinones as therapies and experimental tools. The Journal of Biological Chemistry 2005 280 22 21295 21312 2-s2.0-20444392739 10.1074/jbc.M501527200
80. Murphy M. P., Smith R. A., Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annual Review of Pharmacology and Toxicology 2007 47 629 656 10.1146/annurev.pharmtox.47.120505.105110
81. Skulachev V. P., Antonenko Y. N., Cherepanov D. A., Chernyak B. V., Izyumov D. S., Khailova L. S., Klishin S. S., Korshunova G. A., Lyamzaev K. G., Pletjushkina O. Y., Roginsky V. A., Rokitskaya T. I., Severin F. F., Severina I. I., Simonyan R. A., Skulachev M. V., Sumbatyan N. V., Sukhanova E. I., Tashlitsky V. N., Trendeleva T. A., Vyssokikh M. Y., Zvyagilskaya R. A., Prevention of cardiolipin oxidation and fatty acid cycling as two antioxidant mechanisms of cationic derivatives of plastoquinone (SkQs). Biochimica et Biophysica Acta 2010 1797 6-7 878 889 2-s2.0-77953808603 10.1016/j.bbabio.2010. 03.015
82. Jazwinski S. M., The retrograde response: when mitochondrial quality control is not enough. Biochimica et Biophysica Acta 2013 1833 2 400 409 10.1016/j.bbamcr.2012.02.010
83. Sinclair D. A., Guarente L., Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 1997 91 7 1033 1042 2-s2.0-0031459980 10.1016/S0092- 8674(00)80493-6
84. Jazwinski S. M., The genetics of aging in the yeast Saccharomyces cerevisiae. Genetica 1993 91 1-3 35 51 2-s2.0-0027755545 10.1007/BF01435986
85. Jazwinski S. M., The retrograde response links metabolism with stress responses, chromatin-dependent gene activation, and genome stability in yeast aging. Gene 2005 354 1-2 22 27 2-s2.0-23644443813 10.1016/j.gene.2005.03.040