Home LiteratureArticle Details
PMID: 9096346 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Mitochondrial decay in hepatocytes from old rats: membrane potential declines, heterogeneity and oxidants increase.

Hagen TM, Yowe DL, Bartholomew JC, Wehr CM, Do KL, Park JY, Ames BN

Abstract

Mitochondrial function during aging was assessed in isolated rat hepatocytes to avoid the problem of differential lysis when old, fragile mitochondria are isolated. Rhodamine 123, a fluorescent dye that accumulates in mitochondria on the basis of their membrane potential, was used as a probe to determine whether this key function is affected by aging. A marked fluorescent heterogeneity was observed in hepatocytes from old (20-28 months) but not young (3-5 months) rats, suggesting age-associated alterations in mitochondrial membrane potential, the driving force for ATP synthesis. Three distinct cell subpopulations were separated by centrifugal elutriation; each exhibited a unique rhodamine 123 fluorescence pattern, with the largest population from old rats having significantly lower fluorescence than that seen in young rats. This apparent age-associated alteration in mitochondrial membrane potential was confirmed by measurements with radioactive tetraphenylphosphonium bromide. Cells from young rats had a calculated membrane potential of -154 mV, in contrast to that of the three subpopulations from old rats of -70 mV (the largest population), -93 mV, and -154 mV. Production of oxidants was examined using 2',7'dichlorofluorescin, a dye that forms a fluorescent product upon oxidation. The largest cell subpopulation and a minor one from old animals produced significantly more oxidants than cells from young rats. To investigate the molecular cause(s) for the heterogeneity, we determined the levels of an age-associated mtDNA deletion. No significant differences were seen in the three subpopulations, indicating that the mitochondrial decay is due to other mutations, epigenetic changes, or both.

MeSH Terms
Aging/metabolism Animals DNA, Mitochondrial Flow Cytometry Male Membrane Potentials Mitochondria, Liver/metabolism,physiology Oxidants/metabolism Oxygen/metabolism Rats Rats, Inbred F344 Sequence Deletion
Chemicals
DNA, Mitochondrial Oxidants Oxygen
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Hagen T M
Division of Biochemistry and Molecular Biology, University of California, Berkeley 94720, USA.
Yowe D L
Bartholomew J C
Wehr C M
Do K L
Park J Y
Ames B N
References (30)
30 references, click to expand
  1. Age changes in size and number of mitochondria of human hepatic cells.
    J Gerontol. 1968 Oct;23(4):454-61 PMID: 5723478
  2. Calculation of intracellular pH from the distribution of 5,5-dimethyl-2,4-oxazolidinedione (DMO); application to skeletal muscle of the dog.
    J Clin Invest. 1959 May;38(5):720-9 PMID: 13654506
  3. The effect of age on mitochondrial ultrastructure and enzymes.
    Adv Exp Med Biol. 1975;53:171-83 PMID: 164102
  4. The effect of age on mitochondrial ultrastructure and enzyme cytochemistry.
    Biochem Soc Trans. 1975;3(1):126-8 PMID: 165103
  5. Determination of the mitochondrial protonmotive force in isolated hepatocytes.
    J Biol Chem. 1980 Feb 25;255(4):1458-64 PMID: 7354039
  6. Analysis of viral DNA sequences in hamster cells transformed by herpes simplex virus type 2.
    Proc Natl Acad Sci U S A. 1980 Feb;77(2):880-4 PMID: 6244590
  7. Proliferation of mitochondria during the cell cycle of the human cell line (HL-60).
    J Cell Biol. 1981 May;89(2):256-60 PMID: 7195902
  8. A two-step hypothesis on the mechanisms of in vitro cell aging: cell differentiation followed by intrinsic mitochondrial mutagenesis.
    Exp Gerontol. 1984;19(1):31-6 PMID: 6723817
  9. Use of digitonin fractionation to determine mitochondrial transmembrane ion distribution in cells during anoxia.
    Anal Biochem. 1985 Apr;146(1):164-72 PMID: 3993928
  10. The intracellular distribution of ions and water in rat liver and heart muscle.
    J Microsc. 1987 Apr;146(Pt 1):77-85 PMID: 3599070
  11. Increased uptake and retention of rhodamine 123 by mitochondria of old human fibroblasts.
    Mech Ageing Dev. 1987 Jun;39(1):1-9 PMID: 3613685
  12. A mitochondrial membrane hypothesis of aging.
    J Theor Biol. 1987 Jul 21;127(2):127-32 PMID: 3695544
  13. Normal oxidative damage to mitochondrial and nuclear DNA is extensive.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6465-7 PMID: 3413108
  14. The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates.
    J Mol Evol. 1989 Jun;28(6):497-516 PMID: 2504926
  15. Use of nonyl acridine orange and rhodamine 123 to follow biosynthesis and functional assembly of mitochondrial membrane during L1210 cell cycle.
    Exp Cell Res. 1990 Jan;186(1):130-7 PMID: 1688800
  16. Analysis of cytokine mRNA and DNA: detection and quantitation by competitive polymerase chain reaction.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2725-9 PMID: 2181447
  17. A new method for testing cell ageing using two mitochondria specific fluorescent probes.
    Mech Ageing Dev. 1990 Mar 15;52(2-3):149-67 PMID: 2325431
  18. Correlation of lymphocyte lipid composition membrane microviscosity and mitogen response in the aged.
    Eur J Immunol. 1991 Nov;21(11):2761-5 PMID: 1936121
  19. Separation of two subpopulations of old human fibroblasts by mitochondria (rhodamine 123) fluorescence.
    Growth Dev Aging. 1991 Fall;55(3):185-91 PMID: 1765418
  20. Cardiolipins and biomembrane function.
    Biochim Biophys Acta. 1992 Mar 26;1113(1):71-133 PMID: 1550861
  21. Mitochondrial genetics: a paradigm for aging and degenerative diseases?
    Science. 1992 May 1;256(5057):628-32 PMID: 1533953
  22. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress.
    Chem Res Toxicol. 1992 Mar-Apr;5(2):227-31 PMID: 1322737
  23. Diseases of the mitochondrial DNA.
    Annu Rev Biochem. 1992;61:1175-212 PMID: 1497308
  24. Association of mitochondrial DNA damage with aging and coronary atherosclerotic heart disease.
    Mutat Res. 1992 Sep;275(3-6):169-80 PMID: 1383759
  25. Mitochondrial DNA copy number and mitochondrial DNA deletion in adult and senescent rats.
    Mutat Res. 1992 Sep;275(3-6):181-93 PMID: 1383760
  26. Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain.
    Ann Neurol. 1993 Oct;34(4):609-16 PMID: 8215249
  27. Oxidative damage and mitochondrial decay in aging.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10771-8 PMID: 7971961
  28. Content and fatty acid composition of cardiolipin in the brain of patients with Alzheimer's disease.
    Neurochem Int. 1994 Sep;25(3):295-300 PMID: 7833797
  29. Human epidermal cells progressively lose their cardiolipins during ageing without change in mitochondrial transmembrane potential.
    Mech Ageing Dev. 1994 Dec 16;77(2):83-96 PMID: 7745994
  30. A new multiparameter separator for microscopic particles and biological cells.
    Rev Sci Instrum. 1973 Sep;44(9):1301-10 PMID: 4279087
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-04-01
Pages
3064-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC20322
Subset
IM
Grants
NIEHS NIH HHS · P30 ES001896 · United States
NCI NIH HHS · CA39910 · United States
NIEHS NIH HHS · ES01896 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]