Renin-angiotensin system inhibitors protect against age-related changes in rat liver mitochondrial DNA content and gene expression

Experimental Gerontology

Volumn 43, Issue 10, 2008, Pages 919-928

  de Cavanagh, Elena M V ^a   Flores, Idhaliz ^b   Ferder, Marcelo ^a   Inserra, Felipe ^a   Ferder, León ^b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b PONCE SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

Aging; Anti aging; Antioxidant; Gene expression; Mitochondria DNA; Reactive oxygen species

Indexed keywords

ENALAPRIL; LOSARTAN; MESSENGER RNA; MITOCHONDRIAL DNA; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 20;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENERGY; CONTROLLED STUDY; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA CONTENT; DRUG EFFECT; DRUG INHIBITION; GENE EXPRESSION; LIVER HISTOLOGY; MALE; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; RESPIRATION CONTROL; RESPIRATORY FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AGING; ANIMALS; DNA, MITOCHONDRIAL; GENE EXPRESSION; MALE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RENIN-ANGIOTENSIN SYSTEM;

RATTUS; RODENTIA;

EID: 53049097540     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2008.08.007     Document Type: Article

References (75)

1. Miquel J. An update on the oxygen stress-mitochondrial mutation theory of aging: genetic and evolutionary implications. Exp. Gerontol. 33 (1998) 113-126
2. Krishnan K.J., Greaves L.C., Reeve A.K., and Turnbull D.M. Mitochondrial DNA mutations and aging. Ann. NY Acad. Sci. 1100 (2007) 227-240
3. Yowe D.L., and Ames B.N. Quantitation of age-related mitochondrial DNA deletions in rat tissues shows that their pattern of accumulation differs from that of humans. Gene 209 (1998) 23-30
4. Baumer A., Zhang C., Linnane A.W., and Nagley P. Age-related human mtDNA deletions: a heterogeneous set of deletions arising at a single pair of directly repeated sequences. Am. J. Hum. Genet. 54 (1994) 618-630
5. Lezza A.M., Boffoli D., Scacco S., Cantatore P., and Gadaleta M.N. Correlation between mitochondrial DNA 4977-bp deletion and respiratory chain enzyme activities in aging human skeletal muscles. Biochem. Biophys. Res. Commun. 205 (1994) 772-779
6. Ozawa T. Mechanism of somatic mitochondrial DNA mutations associated with age and diseases. Biochim. Biophys. Acta 1271 (1995) 177-189
7. Phadnis N., Sia R.A., and Sia E.A. Analysis of repeat-mediated deletions in the mitochondrial genome of Saccharomyces cerevisiae. Genetics 171 (2005) 1549-1559
8. Ozawa T. Oxidative Damage and Fragility of Mitochondrial DNA (1999), Marcel Dekker Inc, New York
9. Zeviani M., and Carelli V. Dominance in mitochondrial disorders. J. Inherit. Metab. Dis. 28 (2005) 287-299
10. Srivastava S., and Moraes C.T. Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Hum. Mol. Genet. 14 (2005) 893-902
11. Li J.M., and Shah A.M. Mechanism of endothelial cell NADPH oxidase activation by angiotensin II. Role of the p47phox subunit. J. Biol. Chem. 278 (2003) 12094-12100
12. Mollnau H., Wendt M., Szocs K., Lassegue B., Schulz E., Oelze M., Li H., Bodenschatz M., August M., Kleschyov A.L., Tsilimingas N., Walter U., Forstermann U., Meinertz T., Griendling K., and Munzel T. Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ. Res. 90 (2002) E58-E65
13. Larkin J.E., Frank B.C., Gaspard R.M., Duka I., Gavras H., and Quackenbush J. Cardiac transcriptional response to acute and chronic angiotensin II treatments. Physiol. Genomics 18 (2004) 152-166
14. Munzel T., and Keaney Jr. J.F. Are ACE inhibitors a "magic bullet" against oxidative stress?. Circulation 104 (2001) 1571-1574
15. Toblli J.E., Ferder L., Stella I., Angerosa M., and Inserra F. Enalapril prevents fatty liver in nephrotic rats. J. Nephrol. 15 (2002) 358-367
16. de Cavanagh E.M., Piotrkowski B., Basso N., Stella I., Inserra F., Ferder L., and Fraga C.G. Enalapril and losartan attenuate mitochondrial dysfunction in aged rats. FASEB J. 17 (2003) 1096-1098
17. Ferder L., Inserra F., Romano L., Ercole L., and Pszenny V. Effects of angiotensin-converting enzyme inhibition on mitochondrial number in the aging mouse. Am. J. Physiol. 265 (1993) C15-C18
18. Ferder L.F., Inserra F., and Basso N. Advances in our understanding of aging: role of the renin-angiotensin system. Curr. Opin. Pharmacol. 2 (2002) 189-194
19. Garnier A., Fortin D., Delomenie C., Momken I., Veksler V., and Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J. Physiol. 551 (2003) 491-501
20. Lanni A., Moreno M., Lombardi A., and Goglia F. Biochemical and functional differences in rat liver mitochondrial subpopulations obtained at different gravitational forces. Int. J. Biochem. Cell Biol. 28 (1996) 337-343
21. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
22. Estabrook R. Mitochondrial respiratory control and the polarigraphic measurement of the ADP:O ratios. Methods Enzymol. 10 (1967) 41-47
23. Jones O.T., and Hancock J.T. Assays of plasma membrane NADPH oxidase. Methods Enzymol. 233 (1994) 222-229
24. Knowles R.G., and Salter M. Measurement of NOS activity by conversion of radiolabeled arginine to citrulline using ion-exchange separation. Methods Mol. Biol. 100 (1998) 67-73
25. Flohe L., and Otting F. Superoxide dismutase assays. Methods Enzymol. 105 (1984) 93-104
26. Cassano P., Lezza A.M., Leeuwenburgh C., Cantatore P., and Gadaleta M.N. Measurement of the 4, 834-bp mitochondrial DNA deletion level in aging rat liver and brain subjected or not to caloric restriction diet. Ann. NY Acad. Sci. 1019 (2004) 269-273
27. Serste T., and Bourgeois N. Ageing and the liver. Acta Gastroenterol. Belg. 69 (2006) 296-298
28. Huang S.Z., Luo Y.J., Wang L., and Cai K.Y. Effect of Ginkgo biloba extract on livers in aged rats. World J. Gastroenterol. 11 (2005) 132-135
29. Navarro A., and Boveris A. The mitochondrial energy transduction system and the aging process. Am. J. Physiol. Cell Physiol. 292 (2007) C670-C686
30. Ramanujan V.K., and Herman B.A. Aging process modulates nonlinear dynamics in liver cell metabolism. J. Biol. Chem. 282 (2007) 19217-19226
31. Brandes R.P., Fleming I., and Busse R. Endothelial aging. Cardiovasc. Res. 66 (2005) 286-294
32. Ghafourifar P., and Cadenas E. Mitochondrial nitric oxide synthase. Trends Pharmacol. Sci. 26 (2005) 190-195
33. Elfering S.L., Sarkela T.M., and Giulivi C. Biochemistry of mitochondrial nitric-oxide synthase. J. Biol. Chem. 277 (2002) 38079-38086
34. Brookes P. Mitochondrial nitric oxide synthase. Mitochondrion 3 (2004) 187-204
35. Nakashima H., Suzuki H., Ohtsu H., Chao J.Y., Utsunomiya H., Frank G.D., and Eguchi S. Angiotensin II regulates vascular and endothelial dysfunction: recent topics of Angiotensin II type-1 receptor signaling in the vasculature. Curr. Vasc. Pharmacol. 4 (2006) 67-78
36. Fernandez-Alfonso M.S., and Gonzalez C. Nitric oxide and the renin-angiotensin system. Is there a physiological interplay between the systems?. J. Hypertens. 17 (1999) 1355-1361
37. Nisoli E., Clementi E., Paolucci C., Cozzi V., Tonello C., Sciorati C., Bracale R., Valerio A., Francolini M., Moncada S., and Carruba M.O. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299 (2003) 896-899
38. Czubryt M.P., McAnally J., Fishman G.I., and Olson E.N. Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 α (PGC-1 α) and mitochondrial function by MEF2 and HDAC5. Proc. Natl. Acad. Sci. USA 100 (2003) 1711-1716
39. Nisoli E., Falcone S., Tonello C., Cozzi V., Palomba L., Fiorani M., Pisconti A., Brunelli S., Cardile A., Francolini M., Cantoni O., Carruba M.O., Moncada S., and Clementi E. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc. Natl. Acad. Sci. USA 101 (2004) 16507-16512
40. Piotrkowski B., Fraga C.G., and de Cavanagh E.M. Mitochondrial function and nitric oxide metabolism are modified by enalapril treatment in rat kidney. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 (2007) R1494-R1501
41. Bentlage H.A., and Attardi G. Relationship of genotype to phenotype in fibroblast-derived transmitochondrial cell lines carrying the 3243 mutation associated with the MELAS encephalomyopathy: shift towards mutant genotype and role of mtDNA copy number. Hum. Mol. Genet. 5 (1996) 197-205
42. Nakada K., Inoue K., Ono T., Isobe K., Ogura A., Goto Y.I., Nonaka I., and Hayashi J.I. Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat. Med. 7 (2001) 934-940
43. Nakada K., Ono T., and Hayashi J. A novel defense system of mitochondria in mice and human subjects for preventing expression of mitochondrial dysfunction by pathogenic mutant mtDNAs. Mitochondrion 2 (2002) 59-70
44. Barthelemy C., Ogier de Baulny H., Diaz J., Cheval M.A., Frachon P., Romero N., Goutieres F., Fardeau M., and Lombes A. Late-onset mitochondrial DNA depletion: DNA copy number, multiple deletions, and compensation. Ann. Neurol. 49 (2001) 607-617
45. Moraes C.T. What regulates mitochondrial DNA copy number in animal cells?. Trends Genet. 17 (2001) 199-205
46. Barazzoni R., Short K.R., and 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. 275 (2000) 3343-3347
47. Kang C.M., Kristal B.S., and Yu B.P. Age-related mitochondrial DNA deletions: effect of dietary restriction. Free Radic. Biol. Med. 24 (1998) 148-154
48. Nicklas J.A., Brooks E.M., Hunter T.C., Single R., and Branda R.F. Development of a quantitative PCR (TaqMan) assay for relative mitochondrial DNA copy number and the common mitochondrial DNA deletion in the rat. Environ. Mol. Mutagen. 44 (2004) 313-320
49. Gadaleta M.N., Rainaldi G., Lezza A.M., Milella F., Fracasso F., and Cantatore P. Mitochondrial DNA copy number and mitochondrial DNA deletion in adult and senescent rats. Mutat. Res. 275 (1992) 181-193
50. Enesco H.E., and Samborsky J. Liver polyploidy: influence of age and of dietary restriction. Exp. Gerontol. 18 (1983) 79-87
51. Halle J.P., Muller S., Simm A., and Adam G. Copy number, epigenetic state and expression of the rRNA genes in young and senescent rat embryo fibroblasts. Eur. J. Cell Biol. 74 (1997) 281-288
52. Ekstrand M.I., Falkenberg M., Rantanen A., Park C.B., Gaspari M., Hultenby K., Rustin P., Gustafsson C.M., and Larsson N.G. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 13 (2004) 935-944
53. Scarpulla R.C. Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomembr. 29 (1997) 109-119
54. Finck B.N., and Kelly D.P. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116 (2006) 615-622
55. Spiegelman B.M. Transcriptional control of energy homeostasis through the PGC1 coactivators. Novartis Found Symp. 286 (2007) 3-6 (discusssion 6-12, 162-3, 196-203)
56. Doughan A.K., Harrison D.G., and Dikalov S.I. Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 102 (2008) 488-496
57. Llorens-Cortes C., Greenberg B., Huang H., and Corvol P. Tissular expression and regulation of type 1 angiotensin II receptor subtypes by quantitative reverse transcriptase-polymerase chain reaction analysis. Hypertension 24 (1994) 538-548
58. Speth R.C., and Kim K.H. Discrimination of two angiotensin II receptor subtypes with a selective agonist analogue of angiotensin II, p-aminophenylalanine6 angiotensin II. Biochem. Biophys. Res. Commun. 169 (1990) 997-1006
59. Heymes C., Silvestre J.S., Llorens-Cortes C., Chevalier B., Marotte F., Levy B.I., Swynghedauw B., and Samuel J.L. Cardiac senescence is associated with enhanced expression of angiotensin II receptor subtypes. Endocrinology 139 (1998) 2579-2587
60. Yoshiji, H., Kuriyama, S., Fukui, H., 2007. Blockade of renin-angiotensin system in antifibrotic therapy. J. Gastroenterol. Hepatol. 22 (Suppl. 1), S93-S935.
61. Chan H., Leung P.S., and Tam M.S. Effect of angiotensin AT1 receptor antagonist on d-galactosamine-induced acute liver injury. Clin. Exp. Pharmacol. Physiol. 34 (2007) 985-991
62. Kitami Y., Okura T., Marumoto K., Wakamiya R., and Hiwada K. Differential gene expression and regulation of type-1 angiotensin II receptor subtypes in the rat. Biochem. Biophys. Res. Commun. 188 (1992) 446-452
63. Sechi L.A., Griffin C.A., Giacchetti G., Valentin J.P., Llorens-Cortes C., Corvol P., and Schambelan M. Tissue-specific regulation of type 1 angiotensin II receptor mRNA levels in the rat. Hypertension 28 (1996) 403-408
64. Kimura S., Zhang G.X., Nishiyama A., Shokoji T., Yao L., Fan Y.Y., Rahman M., and Abe Y. Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 45 (2005) 438-444
65. Sorescu D., and Griendling K.K. Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest. Heart Fail. 8 (2002) 132-140
66. Heymes C., Swynghedauw B., and Chevalier B. Activation of angiotensinogen and angiotensin-converting enzyme gene expression in the left ventricle of senescent rats. Circulation 90 (1994) 1328-1333
67. Vincent M., Dupont J., and Sassard J. Plasma renin activity as a function of age in two new strains of spontaneously hypertensive and normotensive rats. Clin. Sci. Mol. Med. 50 (1976) 103-107
68. Belmin J., Levy B.I., and Michel J.B. Changes in the renin-angiotensin-aldosterone axis in later life. Drugs Aging 5 (1994) 391-400
69. Thompson M.M., Oyama T.T., Kelly F.J., Kennefick T.M., and Anderson S. Activity and responsiveness of the renin-angiotensin system in the aging rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000) R1787-R1794
70. Ernsberger P., and Koletsky R.J. Metabolic actions of angiotensin receptor antagonists: PPAR-gamma agonist actions or a class effect?. Curr. Opin. Pharmacol. 7 (2007) 140-145
71. Janke J., Schupp M., Engeli S., Gorzelniak K., Boschmann M., Sauma L., Nystrom F.H., Jordan J., Luft F.C., and Sharma A.M. Angiotensin type 1 receptor antagonists induce human in-vitro adipogenesis through peroxisome proliferator-activated receptor-γ activation. J. Hypertens. 24 (2006) 1809-1816
72. Strazzullo P., and Galletti F. Impact of the renin-angiotensin system on lipid and carbohydrate metabolism. Curr. Opin. Nephrol. Hypertens. 13 (2004) 325-332
73. Casademont J., and Miro O. Electron transport chain defects in heart failure. Heart Fail. Rev. 7 (2002) 131-139
74. Sanbe A., Tanonaka K., Kobayasi R., and Takeo S. Effects of long-term therapy with ACE inhibitors, captopril, enalapril and trandolapril, on myocardial energy metabolism in rats with heart failure following myocardial infarction. J. Mol. Cell. Cardiol. 27 (1995) 2209-2222
75. Wei Y.H., Ma Y.S., Lee H.C., Lee C.F., and Lu C.Y. Mitochondrial theory of aging matures - roles of mtDNA mutation and oxidative stress in human aging. Zhonghua Yi Xue Za Zhi (Taipei) 64 (2001) 259-270