Regulation of mitochondrial biogenesis through TFAM-mitochondrial DNA interactions. Useful insights from aging and calorie restriction studies

Mitochondrion

Volumn 25, Issue , 2015, Pages 67-75

  Picca, Anna ^a   Lezza, Angela Maria Serena ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Aging; Calorie restriction; Mitochondrial biogenesis; MtDNA; TFAM; TFAM mtDNA interactions

Indexed keywords

ESTROGEN RELATED RECEPTOR ALPHA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; DNA BINDING PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

AGING; BIOGENESIS; CALORIC RESTRICTION; DNA REPLICATION; HUMAN; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; METABOLISM; ORGANELLE BIOGENESIS;

AGING; ANIMALS; CALORIC RESTRICTION; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MITOCHONDRIAL PROTEINS; ORGANELLE BIOGENESIS; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 84944241654     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2015.10.001     Document Type: Review

References (105)

1. Ahlqvist K.J., Suomalainen A., Hämäläinen R.H. Stem cells, mitochondria and aging. Biochim. Biophys. Acta 2015, 1847:1380-1386.
2. Anderson R., Prolla T. PGC-1alpha in aging and anti-aging interventions. Biochim. Biophys. Acta 2009, 1790:1059-1066.
3. Anderson R.M., Weindruch R. Metabolic reprogramming, caloric restriction and aging. Trends Endocrinol. Metab. 2010, 21:134-141.
4. Aquilano K., Vigilanza P., Baldelli S., Pagliei B., Rotilio G., Ciriolo M.R. Peroxisome proliferator-activated receptor gamma co-activator 1 alpha (PGC-1α) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J. Biol. Chem. 2010, 285(28):21,590-21,599.
5. Attardi G., Schatz G. Biogenesis of mitochondria. Annu. Rev. Cell Biol. 1988, 4:289-333.
6. Baines H.L., Stewart J.B., Stamp C., Zupanic A., Kirkwood T.B.L., Larsson N.-G., et al. Similar patterns of clonally expanded somatic mtDNA mutations in the colon of heterozygous mtDNA mutator mice and ageing humans. Mech. Ageing Dev. 2014, 139:22-30.
7. Barazzoni R., Short K.R., Nair K.S. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J. Biol. Chem. 2000, 275:3343-3347.
8. Barja G. Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Res. 2007, 10:215-224.
9. Bender T., Lewrenz I., Franken S., Baitzel C., Voos W. Mitochondrial enzymes are protected from stress-induced aggregation by mitochondrial chaperones and the Pim1/LON protease. Mol. Biol. Cell 2011, 22:541-554.
10. Bestwick M.L., Shadel G.S. Accessorizing the human mitochondrial transcription machinery. Trends Biochem. Sci. 2013, 38:283-291.
11. Bogenhagen D.F. Mitochondrial DNA nucleoid structure. Biochim. Biophys. Acta 2012, 1819:914-920.
12. Bogenhagen D.F., Rousseau D., Burke S. The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 2008, 283:3665-3675.
13. Bonawitz N.D., Clayton D.A., Shadel G.S. Initiation and beyond: multiple functions of the human mitochondrial transcription machinery. Mol. Cell 2006, 24:813-825.
14. Brown T.A., Cecconi C., Tkachuk A.N., Bustamante C., Clayton D.A. Replication of mitochondrial DNA occurs by strand displacement with alternative light-strand origins, not via a strand-coupled mechanism. Genes Dev. 2005, 19:2466-2476.
15. Campbell C.T., Kolesar J.E., Kaufman B.A. Mitochondrial transcription factor A regulates mitochondrial transcription initiation, DNA packaging, and genome copy number. Biochim. Biophys. Acta 2012, 1819:921-929.
16. Canugovi C., Maynard S., Bayne A.C., Sykora P., Tian J., Souza-Pinto N.C., et al. The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair (Amst) 2010, 9:1080-1089.
17. Cassano P., Sciancalepore A.G., Lezza A.M., Leeuwenburgh C., Cantatore P., Gadaleta M.N. Tissue-specific effect of age and caloric restriction diet on mitochondrial DNA content. Rejuvenation Res. 2006, 9:211-214.
18. Chang D.D., Clayton D.A. Priming of human mitochondrial DNA replication occurs at the light-strand promoter. Proc. Natl. Acad. Sci. U. S. A. 1985, 82(2):351-355.
19. Chang D.D., Hauswirth W.W., Clayton D.A. Replication priming and transcription initiate from precisely the same site in mouse mitochondrial DNA. EMBO J. 1985, 4(6):1559-1567.
20. Correia-Melo C., Passos J.F. Mitochondria: are they causal players in cellular senescence?. Biochim. Biophys. Acta 2015, 1847:1373-1379.
21. Cotney J., Wang Z., Shadel G.S. Relative abundance of the human mitochondrial transcription system and distinct roles for h-mtTFB1 and h-mtTFB2 in mitochondrial biogenesis and gene expression. Nucleic Acids Res. 2007, 35:4042-4054.
22. Dairaghi D.J., Shadel G.S., Clayton D.A. Addition of a 29 residue carboxyl-terminal tail converts a simple HMG box-containing protein into a transcriptional activator. J. Mol. Biol. 1995, 249:11-28.
23. Dairaghi D.J., Shadel G.S., Clayton D.A. Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim. Biophys. Acta 1995, 1271:127-134.
24. Dinardo M.M., Musicco C., Fracasso F., Milella F., Gadaleta M.N., Gadaleta G., et al. Acetylation and level of mitochondrial transcription factor A in several organs of young and old rats. Biochem. Biophys. Res. Commun. 2003, 301:187-191.
25. Ekstrand M.I., Falkenberg M., Rantanen A., Park C.B., Gaspari M., Hultenby K., et al. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 2004, 13:935-944.
26. Falkenberg M., Gaspari M., Rantanen A., Trifunovic A., Larsson N.-G., Gustafsson C.M. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 2002, 31:289-294.
27. Farge G., Laurens N., Broekmans O.D., van den Wildenberg S.M., Dekker L.C., Gaspari M., et al. Protein sliding and DNA denaturation are essential for DNA organization by human mitochondrial transcription factor A. Nat. Commun. 2012, 3:1013.
28. Farge G., Mehmedovic M., Baclayon M., van den Wildenberg S.M.J.L., Roos V.H., Gustfsson C.M., et al. In vitro-reconstituted nucleoids can block mitochondrial DNA replication and transcription. Cell Rep. 2014, 8:1-9.
29. Finck B.N., Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Investig. 2006, 116:615-622.
30. Fisher R.P., Clayton D.A. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol. 1988, 8:3496-3509.
31. Fisher R.P., Topper J.N., Clayton D.A. Promoter selection in human mitochondria involves binding of a transcription factor to orientation-independent upstream regulatory elements. Cell 1987, 50:247-258.
32. Fisher R.P., Parisi M.A., Clayton D.A. Flexible recognition of rapidly evolving promoter sequences by mitochondrial transcription factor 1. Genes Dev. 1989, 3:2202-2217.
33. Fisher R.P., Lisowsky T., Parisi M.A., Clayton D.A. DNA wrapping and bending by a mitochondrial high mobility group-like transcriptional activator protein. J. Biol. Chem. 1992, 267:3358-3367.
34. Fontana L. The scientific basis of caloric restriction leading to longer life. Curr. Opin. Gastroenterol. 2009, 25:144-150.
35. Freyer C., Park C.B., Ekstrand M.I., Shi Y., Khvorostova J., Wibom R., et al. Maintenance of respiratory chain function in mouse hearts with severely impaired mtDNA transcription. Nucleic Acids Res. 2010, 38:6577-6588.
36. Fusté J.M., Wanrooij S., Jemt E., Granycome C.E., Cluett T.J., Shi Y., et al. Mitochondrial RNA polymerase is needed for activation of the origin of light-strand DNA replication. Mol. Cell 2010, 37(1):67-78.
37. Gadaleta M.N., Petruzzella V., Renis M., Fracasso F., Cantatore P. Reduced transcription of mitochondrial DNA in the senescent rat. Tissue dependence and effect of l-carnitine. Eur. J. Biochem. 1990, 187:501-506.
38. Greaves L.C., Nooteboom M., Elson J.L., Tuppen H.A.L., Taylor G.A., Commane D.M., et al. Clonal expansion of early to mid-life mitochondrial DNA point mutations drives mitochondrial dysfunction during human ageing. PLoS Genet. 2014, 10. 10.1371/journal.pgen.1004620.
39. Guarente L. Mitochondria - a nexus for aging, calorie restriction, and sirtuins?. Cell 2008, 132:171-176.
40. Handschin C., Spiegelman B.M. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 2006, 27:728-735.
41. Hayashi Y., Yoshida M., Yamato M., Ide T., Wu Z., Ochi-Shindou M., et al. Reverse of age-dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor A in mice. J. Neurosci. 2008, 28:8624-8634.
42. Hebert A.S., Dittenhafer-Reed K.E., Yu W., Bailey D.J., Selen E.S., Boersma M.D., et al. Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol. Cell 2013, 49:186-199.
43. Holt I.J., Lorimer H.E., Jacobs H.T. Coupled leading- and lagging strand synthesis of mammalian mitochondrial DNA. Cell 2000, 100:515-524.
44. Ikeuchi M., Matsusaka H., Kang D., Matsushima S., Ide T., Kubota T., et al. Overexpression of mitochondrial transcription factor A ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 2005, 112:683-690.
45. Joseph A.M., Rungi A.A., Robinson B.H., Hood D.A. Compensatory responses of protein import and transcription factor expression in mitochondrial DNA defects. Am. J. Physiol. Cell Physiol. 2004, 286(4):C 867-C 875.
46. Kanki T., Ohgaki K., Gaspari M., Gustafsson C.M., Fukuoh A., Sasaki, et al. Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol. Cell. Biol. 2004, 24:9823-9834.
47. Kaufman B.A., Durisic N., Mativetsky J.M., Costantino S., Hancock M.A., Grutter P., et al. The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol. Biol. Cell 2007, 18:3225-3236.
48. Kauppila J.H.K., Stewart J.B. Mitochondrial DNA: radically free of free-radical driven mutations. Biochim. Biophys. Acta 2015, 1847:1354-1361.
49. Keeney P.M., Quigley C.K., Dunham L.D., Papageorge C.M., Iyer S., Thomas R.R., et al. Mitochondrial gene therapy augments mitochondrial physiology in a Parkinson's disease cell model. Hum. Gene Ther. 2009, 20:897-907.
50. Kukat C., Wurm C.A., Spahr H., Falkenberg M., Larsson N.-G., Jakobs S. Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:13534-13539.
51. Kukat C., Davies K.M., Wurm C.A., Spåhr H., Bonekamp N.A., Kühl I., et al. Cross-strand binding of TFAM to a single mtDNA molecule forms the mitochondrial nucleoid. PNAS 2015, 112:11288-11293.
52. Larsson N.-G., Wang J., Wilhelmsson H., Oldfors A., Rustin P., Lewandoski M., et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 1998, 18:231-236.
53. Lin J., Puigserver P., Donovan J., Tarr P., Spiegelman B.M. Peroxisome proliferator-activated receptor gamma coactivator 1beta (PGC-1beta), a novel PGC-1-related transcription coactivator associated with host cell factor. J. Biol. Chem. 2002, 277:1645-1648.
54. Litonin D., Sologub M., Shi Y., Savkina M., Anikin M., Falkenberg M., et al. Human mitochondrial transcription revisited: only TFAM and TFB2M are required for transcription of the mitochondrial genes in vitro. J. Biol. Chem. 2010, 285:18129-18133.
55. Liu T., Lu B., Lee I., Ondrovicová G., Kutejová E., Suzuki C.K. DNA and RNA binding by the mitochondrial lon protease is regulated by nucleotide and protein substrate. J. Biol. Chem. 2004, 279:13902-13910.
56. Lodeiro M.F., Uchida A., Bestwick M., Moustafa I.M., Arnold J.J., Shadel G.S., et al. Transcription from the second heavy-strand promoter of human mtDNA is repressed by transcription factor A in vitro. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6513-6518.
57. Lu B., Yadav S., Shah P.G., Liu T., Tian B., Pukszta S., et al. Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance. J. Biol. Chem. 2007, 282:17363-17374.
58. Lu B., Lee J., Nie X., Li M., Morozov Y.I., Venkatesh S., et al. Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+ Lon protease. Mol. Cell 2013, 49:121-132.
59. Maniura-Weber K., Goffart S., Garstka H.L., Montoya J., Wiesner R.J. Transient overexpression of mitochondrial transcription factor A (TFAM) is sufficient to stimulate mitochondrial DNA transcription, but not sufficient to increase mtDNA copy number in cultured cells. Nucleic Acids Res. 2004, 32:6015-6027.
60. Masoro E.J. Overview of caloric restriction and ageing: an update. Mech. Ageing Dev. 2005, 126:913-922.
61. Matsushima Y., Goto Y.-I., Kaguni L.S. Mitochondrial Lon protease regulates mitochondrial DNA copy number and transcription by selective degradation of mitochondrial transcription factor A (TFAM). Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18410-18415.
62. Mirebeau-Prunier D., Le Pennec S., Jacques C., Gueguen N., Poirier J., Malthiery Y., et al. Estrogen-related receptor alpha and PGC-1-related coactivator constitute a novel complex mediating the biogenesis of functional mitochondria. FEBS J. 2010, 277:713-725.
63. Navarro A., Boveris A. Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287(543):R1244-R1249.
64. Ngo H.B., Kaiser J.T., Chan D.C. The mitochondrial transcription and packaging factor Tfam imposes a U-turn on mitochondrial DNA. Nat. Struct. Mol. Biol. 2011, 18:1290-1296.
65. Noack H., Bednarek T., Heidler J., Ladig R., Holtz J., Szibor M. TFAM-dependent and independent dynamics of mtDNA levels in C2C12 myoblasts caused by redox stress. Biochim. Biophys. Acta 2006, 1760:141-150.
66. Ohgaki K., Kanki T., Fukuoh A., Kurisaki H., Aoki Y., Ikeuchi M., et al. The C-terminal tail of mitochondrial transcription factor A markedly strengthens its general binding to DNA. J. Biol. Chem. 2007, 141:201-211.
67. Parisi M.A., Clayton D.A. Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 1991, 252:965-969.
68. Park S.K., Prolla T.A. Lessons learned from gene expression profile studies of aging and caloric restriction. Ageing Res. Rev. 2005, 4:55-65.
69. Pastukh V., Shokolenko I., Wang B., Wilson G., Alexeyev M. Human mitochondrial transcription factor A possesses multiple subcellular targeting signals. FEBS J. 2007, 274:6488-6499.
70. Payne B.A., Chinnery P.F. Mitochondrial dysfunction in aging: much progress but many unresolved questions. Biochim. Biophys. Acta 2015, 1847:1347-1353.
71. Peralta S., Wang X., Moraes C.T. Mitochondrial transcription: lessons from mouse models. Biochim. Biophys. Acta 2012, 1819(9-10):961-969.
72. Pesce V., Cormio A., Fracasso F., Lezza A.M., Cantatore P., Gadaleta M.N. Age-related changes of mitochondrial DNA content and mitochondrial genotypic and phenotypic alterations in rat hind-limb skeletal muscles. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2005, 60:715-723.
73. Philp A., Belew M.Y., Evans A., Pham D., Silvia I., Chen A., et al. The PGC-1{alpha}-related co-activator (PRC) promotes mitochondrial and myogenic adaptations in C2C12 myotubes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301:864-872.
74. Picca A., Pesce V., Fracasso F., Joseph A.-M., Leeuwenburgh C., Lezza A.M.S. Aging and calorie restriction oppositely affect mitochondrial biogenesis through TFAM binding at both origins of mitochondrial DNA replication in rat liver. PLoS One 2013, 8(9).
75. Picca A., Fracasso F., Pesce V., Cantatore P., Joseph A.-M., Leeuwenburgh C., et al. Age- and calorie restriction-related changes in rat brain mitochondrial DNA and TFAM binding. AGE 2013, 35:1607-1620.
76. Picca A., Pesce V., Fracasso F., Joseph A.-M., Leeuwenburgh C., Lezza A.M.S. A comparison among the tissue-specific effects of aging and calorie restriction on TFAM amount and TFAM-binding activity to mtDNA in rat. Biochim. Biophys. Acta 2014, 1840(7):2184-2191.
77. Pinto M., Moraes C.T. Mechanisms linking mtDNA damage and aging. Free Radic. Biol. Med. 2015, 85:250-258.
78. Pohjoismäki J.L.O., Wanrooij S., Hyvärinen A.K., Goffart S., Holt I.J., Spelbrink J.N., et al. Alterations to the expression level of mitochondrial transcription factor A, TFAM, modify the mode of mitochondrial DNA replication in cultured human cells. Nucleic Acids Res. 2006, 34:5815-5828.
79. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
80. Rebelo A.P., Dillon L.M., Moraes C.T. Mitochondrial DNA transcription regulation and nucleoid organization. J. Inherit. Metab. Dis. 2011, 34:941-951.
81. Ristow M., Schmeisser S. Extending life span by increasing oxidative stress. Free Radic. Biol. Med. 2011, 51:327-336.
82. Rubio-Cosials A., Sidow J.F., Jiménez-Menéndez N., Fernandez-Millan P., Montoja J., Jacobs H.T., et al. Human mitochondrial transcription factor A induces a U-turn structure in the light strand promoter. Nat. Struct. Mol. Biol. 2011, 18:1281-1289.
83. Ruetenik A., Barrientos A. Dietary restriction, mitochondrial function and aging: from yeast to humans. Biochim. Biophys. Acta 2015, 1847:1434-1447.
84. Rugarli E., Trifunovic A. Is mitochondrial free radical theory of aging getting old?. Biochim. Biophys. Acta 2015, 1847:1345-1346.
85. Safdar A., Little J.P., Stokl A.J., Hettinga B.P., Akhtar M., Tarnopolsky M.A. Exercise increases mitochondrial PGC-1α content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J. Biol. Chem. 2011, 286(12):10,605-10,617.
86. Saleem A., Hood D.A. Acute exercise induces tumour suppressor protein p53 translocation to the mitochondrial and promotes a p53-Tfam-mitochondrial DNA complex in skeletal muscle. J. Physiol. 2013, 591(14):3625-3636.
87. Santos J.M., Mishra M., Kowluru R.A. Post-translational modification of mitochondrial transcription factor A in impaired mitochondria biogenesis: implications in diabetic retinopathy and metabolic memory phenomenon. Exp. Eye Res. 2014, 121:168-177.
88. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 2008, 88:611-638.
89. Schreiber S.N., Knutti D., Brogli K., Uhlmann T., Kralli A. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor alpha (ERRalpha). J. Biol. Chem. 2003, 278:9013-9018.
90. Schroeder E.A., Raimundo N., Shadel G.S. Epigenetic silencing mediates mitochondria stress-induced longevity. Cell Metab. 2013, 17:954-964.
91. Shi Y., Chan D.W., Jung S.Y., Malovannaya A., Wang Y., Qin J. A data set of human endogenous protein ubiquitination sites. Mol. Cell. Proteomics 2011, 10. (M110.002089).
92. Shi Y., Dierckx A., Wanrooij P.H., Wanrooij S., Larsson N.-G., Wilhelmsson L.M., et al. Mammalian transcription factor A is a core component of the mitochondrial transcription machinery. PNAS 2012, 109:16510-16515.
93. Shutt T.E., Lodeiro M.F., Cotney J., Cameron C.E., Shadel G.S. Core human mitochondrial transcription apparatus is a regulated two-component system in vitro. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:12133-12138.
94. Shutt T.E., Bestwick M., Shadel G.S. The core human mitochondrial transcription initiation complex: it only takes two to tango. Transcription 2011, 2:55-59.
95. Szczepanowska K., Trifunovic A. Different faces of mitochondrial DNA mutators. Biochim. Biophys. Acta 2015, 1847:1362-1372.
96. Takamatsu C., Umeda S., Ohsato T., Ohno T., Abe Y., Fukuoh A., et al. Regulation of mitochondrial D-loops by transcription factor A and single-stranded DNA-binding protein. EMBO Rep. 2002, 3:451-456.
97. Virbasius C.A., Virbasius J.V., Scarpulla R.C. NRF-1, an activator involved in nuclear-mitochondrial interactions, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Genes Dev. 1993, 7:2431-2445.
98. Virbasius J.V., Virbasius C.A., Scarpulla R.C. Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev. 1993, 7:380-392.
99. Wallace D.C. Mitochondrial genetics: a paradigm for aging and degenerative diseases?. Science 1992, 256:628-632.
100. Wang Y.E., Marinov G.K., Wold B.J., Chan D.C. Genome-wide analysis reveals coating of the mitochondrial genome by TFAM. PLoS One 2013, 8(8).
101. Wang K.Z., Zhu J., Dagda R.K., Uechi G., Cherra S.J., Gusdon A.M., et al. ERK-mediated phosphorylation of TFAM downregulates mitochondrial transcription: implications for Parkinson's disease. Mitochondrion 2014, 17:132-140.
102. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
103. Yang M.Y., Bowmaker M., Reyes A., Vergani L., Angeli P., Gringeri E., et al. Biased incorporation of ribonucleotides on the mitochondrial L-strand accounts for apparent strand-asymmetric DNA replication. Cell 2002, 111:495-505.
104. Yasukawa T., Yang M.Y., Jacobs H.T., Holt I.J. A bidirectional origin of replication maps to the major noncoding region of human mitochondrial DNA. Mol. Cell 2005, 18:651-662.
105. Zollo O., Tiranti V., Sondheimer N. Transcriptional requirements of the distal heavy-strand promoter of mtDNA. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6508-6512.