Aging and Calorie Restriction Oppositely Affect Mitochondrial Biogenesis through TFAM Binding at Both Origins of Mitochondrial DNA Replication in Rat Liver

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Picca, Anna ^a   Pesce, Vito ^b   Fracasso, Flavio ^b   Joseph, Anna Maria ^a   Leeuwenburgh, Christiaan ^a   Lezza, Angela M S ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXIREDOXIN 3; REACTIVE OXYGEN METABOLITE;

AGE DISTRIBUTION; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOGENESIS; CALORIC RESTRICTION; CONTROLLED STUDY; DNA REPLICATION; GENE EXPRESSION REGULATION; GENETIC CORRELATION; IN VIVO STUDY; LIVER METABOLISM; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN DNA BINDING; RAT;

AGING; ANIMALS; CALORIC RESTRICTION; DNA REPLICATION; DNA, MITOCHONDRIAL; IMMUNOPRECIPITATION; LIVER; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIAL TURNOVER; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RATS; REACTIVE OXYGEN SPECIES; REPLICATION ORIGIN; TRANSCRIPTION FACTORS;

EID: 84884149486     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074644     Document Type: Article

References (57)

1. Wallace DC, (1992) Mitochondrial genetics: a paradigm for aging and degenerative diseases? Science 256: 628-632. doi:10.1126/science.1533953. PubMed: 1533953.
2. Huang JH, Hood DA, (2009) Age-associated mitochondrial dysfunction in skeletal muscle: Contributing factors and suggestions for long-term interventions. IUBMB Life 61: 201-214. doi:10.1002/iub.164. PubMed: 19243006.
3. Navarro A, Boveris A, (2010) Brain mitochondrial dysfunction in aging, neurodegeneration, and Parkinson's disease. Front Aging Neurosci 2: 1-11. PubMed: 20552041.
4. Navarro A, Boveris A, (2007) The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 292: C670-C686. PubMed: 17020935.
5. Harman D, (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20: 145-147. PubMed: 5016631.
6. Miguel J, Fleming JE, (1986) Theoretical and experimental support for an "oxygen radical mitochondrial injury" hypothesis of cell aging. In: Johnson J, Walford R, Harman D, Miquel J, eds. Free Radicals, Aging, and Degenerative Diseases. ALAN Rev Liss: pp. 51-74.
7. Linnane AW, Marzuki S, Ozawa T, Tanaka M, (1989) Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet 1: 642-645. PubMed: 2564461.
8. Druzhyna NM, Wilson GL, LeDoux SP, (2008) Mitochondrial DNA repair in aging and disease. Mech Ageing Dev 129: 383-390. doi:10.1016/j.mad.2008.03.002. PubMed: 18417187.
9. Barrientos A, Casademont J, Cardellach F, Estivill X, Urbano-Marquez A, et al. (1997) Reduced steady-state levels of mitochondrial RNA and increased mitochondrial DNA amount in human brain with aging. Brain Res. Mol Brain Res 52: 284-289. doi:10.1016/S0169-328X(97)00278-7. PubMed: 9495550.
10. Barazzoni R, Short KR, Nair KS, (2000) Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J Biol Chem 275: 3343-3347. doi:10.1074/jbc.275.5.3343. PubMed: 10652323.
11. Pesce V, Cormio A, Fracasso F, Vecchiet J, Felzani G, et al. (2001) Age-related mitochondrial genotypic and phenotypic alterations in human skeletal muscle. Free Radic Biol Med 30: 1223-1233. doi:10.1016/S0891-5849(01)00517-2. PubMed: 11368920.
12. McInerny SC, Brown AL, Smith DW, (2009) Region-specific changes in mitochondrial D-loop in aged rat CNS. Mech Ageing Dev 130: 343-349. doi:10.1016/j.mad.2009.01.008. PubMed: 19428453.
13. Picca A, Fracasso F, Pesce V, Cantatore P, Joseph AM, et al.Age- and calorie restriction-related changes in rat brain mitochondrial DNA and TFAM binding. Dordr: AGE. doi:10.1007/s11357-012-9465-z Sep 4(2012) [Epub ahead of print].
14. Cassano P, Sciancalepore AG, Lezza AM, Leeuwenburgh C, Cantatore P, et al. (2006) Tissue-specific effect of age and caloric restriction diet on mitochondrial DNA content. Rejuvenation Res 9: 211-214. doi:10.1089/rej.2006.9.211. PubMed: 16706645.
15. Pesce V, Nicassio L, Fracasso F, Musicco C, Cantatore P, et al. (2012) Acetyl-L-carnitine activates the peroxisome proliferator-activated receptor-γ coactivators PGC-1α/ PGC-1β-dependent signaling cascade of mitochondrial biogenesis and decreases the oxidized peroxiredoxins content in old rat liver. Rejuvenation Res 15: 136-139. doi:10.1089/rej.2011.1255. PubMed: 22533417.
16. Sahin E, DePinho RA, (2012) Axis of ageing: telomeres, p53 and mitochondria. Nat Rev Mol Cell Biol 13: 397-404. doi:10.1038/nrm3352. PubMed: 22588366.
17. Kanki T, Ohgaki K, Gaspari M, Gustafsson CM, Fukuoh A, et al. (2004) Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol Cell Biol 24: 9823-9834. doi:10.1128/MCB.24.22.9823-9834.2004. PubMed: 15509786.
18. Lezza AMS, (2012) Mitochondrial transcription factor A (TFAM): one actor for different roles. Front Biol 7: 30-39. doi:10.1007/s11515-011-1175-x.
19. Fisher RP, Clayton DA, (1988) Purification and characterization of human mitochondrial transcription factor 1. Mol Cell Biol 8: 3496-3509. PubMed: 3211148.
20. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, et al. (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18: 231-236. doi:10.1038/ng0398-231. PubMed: 9500544.
21. Parisi MA, Clayton DA, (1991) Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252: 965-969. doi:10.1126/science.2035027. PubMed: 2035027.
22. Kaufman BA, Durisic N, Mativetsky JM, Costantino S, Hancock MA, et al. (2007) The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol Biol Cell 18: 3225-3236. doi:10.1091/mbc.E07-05-0404. PubMed: 17581862.
23. Yoshida Y, Izumi H, Ise T, Uramoto H, Torigoe T, et al. (2002) Human mitochondrial transcription factor A binds preferentially to oxidatively damaged DNA. Biochem Biophys Res Commun 295: 945-951. doi:10.1016/S0006-291X(02)00757-X. PubMed: 12127986.
24. Canugovi C, Maynard S, Bayne AC, Sykora P, Tian J, et al. (2010) The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair 9: 1080-1089. doi:10.1016/j.dnarep.2010.07.009. PubMed: 20739229.
25. Dinardo MM, Musicco C, Milella F, Gadaleta MN, et al. (2003) Acetylation and level of mitochondrial transcription factor A in several organs of young and old rats. Biochem Biophys Res Commun 301: 187-191. doi:10.1016/S0006-291X(02)03008-5. PubMed: 12535660.
26. Pesce V, Cormio A, Fracasso F, Lezza AM, Cantatore P, et al. (2005) Age-related changes of mitochondrial DNA content and mitochondrial genotypic and phenotypic alterations in rat hind-limb skeletal muscles. J Gerontol A Biol Sci Med Sci 60: 715-723. doi:10.1093/gerona/60.6.715. PubMed: 15983173.
27. Masoro EJ, (2000) Caloric restriction and aging: an update. Exp Gerontol 35: 299-305. doi:10.1016/S0531-5565(00)00084-X. PubMed: 10832051.
28. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, et al. (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLOS Med 4: e76. doi:10.1371/journal.pmed.0040076. PubMed: 17341128.
29. Guarente L, (2008) Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell 132: 171-176. doi:10.1016/j.cell.2008.01.007. PubMed: 18243090.
30. Barja G, (2007) Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuvenation Res 10: 215-224. doi:10.1089/rej.2006.0516. PubMed: 17523876.
31. Aspnes LE, Lee CM, Weindruch R, Chung SS, Roecker EB, et al. (1997) Caloric restriction reduces fiber loss and mitochondrial abnormalities in aged rat muscle. FASEB J 11: 573-581. PubMed: 9212081.
32. Kang CM, Kristal BS, Yu BP, (1998) Age-related mitochondrial DNA deletions: effect of dietary restriction. Free Radic Biol Med 24: 148-154. doi:10.1016/S0891-5849(97)00204-9. PubMed: 9436624.
33. Gredilla R, Barja G, López-Torres M, (2001) Effect of short-term caloric restriction on H2O2 production and oxidative DNA damage in rat liver mitochondria and location of the free radical source. J Bioenerg Biomembr 33: 279-287. doi:10.1023/A:1010603206190. PubMed: 11710804.
34. López-Torres M, Gredilla R, Sanz A, Barja G, (2002) Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med 32: 882-889. doi:10.1016/S0891-5849(02)00773-6. PubMed: 11978489.
35. Cassano P, Lezza AM, Leeuwenburgh C, Cantatore P, Gadaleta MN, (2004) Measurement of the 4,834-bp mitochondrial DNA deletion level in aging rat liver and brain subjected or not to caloric restriction diet. Ann N Y Acad Sci 1019: 269-273. doi:10.1196/annals.1297.045. PubMed: 15247027.
36. Stuart JA, Karahalil B, Hogue BA, Souza-Pinto NC, Bohr VA, (2004) Mitochondrial and nuclear DNA base excision repair are affected differently by caloric restriction. FASEB J 18: 595-597. PubMed: 14734635.
37. Bua E, McKiernan SH, Aiken JM, (2004) Calorie restriction limits the generation but not the progression of mitochondrial abnormalities in aging skeletal muscle. FASEB J 18: 582-584. PubMed: 14734641.
38. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time PCR. Nucleic Acids Res 29: e45. doi:10.1093/nar/29.9.e45. PubMed: 11328886.
39. Vercauteren K, Pasko RA, Gleyzer N, Marino VM, Scarpulla RC, (2006) 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: 7409-7419. doi:10.1128/MCB.00585-06. PubMed: 16908542.
40. Anderson RM, Barger JL, Edwards MG, Braun KH, O'Connor CE, et al. (2008) Dynamic regulation of PGC-1α localization and turnover implicates mitochondrial adaptation in calorie restriction and the stress response. Aging Cell 7: 101-111. doi:10.1111/j.1474-9726.2007.00357.x. PubMed: 18031569.
41. Scarpulla RC, (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14. doi:10.1016/S0167-4781(02)00343-3. PubMed: 12031478.
42. Chang TS, Cho CS, Park S, Yu S, Kang SW, Rhee SG, (2004) Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J Biol Chem 279: 41975-41984. doi:10.1074/jbc.M407707200. PubMed: 15280382.
43. Musicco C, Capelli C, Pesce V, Timperio AM, Calvani M, et al. (2009) Accumulation of overoxidized Peroxiredoxin III in aged rat liver mitochondria. Biochim Biophys Acta 1787: 890-896. doi:10.1016/j.bbabio.2009.03.002. PubMed: 19272351.
44. Storz P, Döppler H, Toker A, (2005) Protein kinase D mediates mitochondrion-to-nucleus signaling and detoxification from mitochondrial reactive oxygen species. Mol Cell Biol 25: 8520-8530. doi:10.1128/MCB.25.19.8520-8530.2005. PubMed: 16166634.
45. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, et al. (2006) Suppression of reactive oxygen species and neurodegeneration by the PGC-1α transcriptional coactivators. Cell 127: 397-408. doi:10.1016/j.cell.2006.09.024. PubMed: 17055439.
46. Paradies G, Petrosillo G, Paradies V, Ruggiero FM, (2010) Oxidative stress, mitochondrial bioenergetics, and cardiolipin in aging. Free Radic Biol Med 48: 1286-1295. doi:10.1016/j.freeradbiomed.2010.02.020. PubMed: 20176101.
47. Woo DK, Green PD, Santos JH, D'Souza AD, Walther Z, Martin WD, Christian BE, Chandel NS, Shadel GS, (2012) Mitochondrial genome instability and ROS enhance intestinal tumorigenesis in APC (Min/+) mice. Am J Pathol 180: 24-31. doi:10.1016/j.ajpath.2011.10.003. PubMed: 22056359.
48. Van Houten B, Woshner V, Santos JH, (2006) Role of mitochondrial DNA in toxic responses to oxidative stress. DNA Repair (Amst) 5: 145-152. doi:10.1016/j.dnarep.2005.03.002. PubMed: 15878696.
49. Huh JY, Kim Y, Jeong J, Park J, Kim I, et al. (2012) Peroxiredoxin 3 is a key molecule regulating adipocyte oxidative stress, mitochondrial biogenesis, and adipokine expression. Antioxid Redox Signal 16: 229-243. doi:10.1089/ars.2010.3766. PubMed: 21902452.
50. Chiribau CB, Cheng L, Cucoranu IC, Yu YS, Clempus RE, et al. (2008) FOXO3A regulates peroxiredoxin III expression in human cardiac fibroblasts. J Biol Chem 283: 8211-8217. doi:10.1074/jbc.M710610200. PubMed: 18195003.
51. Hwang IK, Yoo KY, Kim DW, Lee CH, Choi JH, et al. (2010) Changes in the expression of mitochondrial peroxiredoxin and thioredoxin in neurons and glia and their protective effects in experimental cerebral ischemic damage. Free Radic Biol Med 48: 1242-1251. doi:10.1016/j.freeradbiomed.2010.02.007. PubMed: 20156553.
52. Dairaghi DJ, Shadel GS, Clayton DA, (1995) Human mitochondrial transcription factor A and promoter spacing integrity are required for transcription initiation. Biochim Biophys Acta 1271: 127-134. doi:10.1016/0925-4439(95)00019-Z. PubMed: 7599198.
53. Lodeiro MF, Uchida A, Bestwick M, Moustafa IM, Arnold JJ, et al. (2012) 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 109: 6513-6518. doi:10.1073/pnas.1118710109. PubMed: 22493245.
54. Zollo O, Tiranti V, Sondheimer N, (2012) Transcriptional requirements of the distal heavy-strand promoter of mtDNA. Proc Natl Acad Sci U S A 109: 6508-6512. doi:10.1073/pnas.1118594109. PubMed: 22454497.
55. Shutt TE, Bestwick M, Shadel GS, (2011) The core human mitochondrial transcription initiation complex. It only takes two to tango. Transcription 2: 55-59. doi:10.4161/trns.2.2.14296. PubMed: 21468229.
56. Gadaleta MN, Petruzzella V, Renis M, Fracasso F, Cantatore P, (1990) Reduced transcription of mitochondrial DNA in the senescent rat. Tissue dependence and effect of L-carnitine. Eur J Biochem 187: 501-506. doi:10.1111/j.1432-1033.1990.tb15331.x. PubMed: 2154375.
57. Hebert AS, Dittenhafer-Reed KE, Yu W, Bailey DJ, Selen ES, et al. (2013) Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol Cell 49: 186-199. PubMed: 23201123.