Evaluation of sex differences on mitochondrial bioenergetics and apoptosis in mice

Experimental Gerontology

Volumn 42, Issue 3, 2007, Pages 173-182

  Sanz, Alberto ^a   Hiona, Asimina ^b   Kujoth, Gregory C ^c   Seo, Arnold Y ^b   Hofer, Tim ^b   Kouwenhoven, Evelyn ^b   Kalani, Rizwan ^b   Prolla, Tomas A ^c   Barja, Gustavo ^a   Leeuwenburgh, Christiaan ^b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b Department of Clinical and Health Psychology   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apoptosis; Females; Males; Mitochondria; Mitochondrial DNA; Oxidative stress

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ADENOSINE TRIPHOSPHATE; CARBONYL DERIVATIVE; CASPASE 3; CASPASE 9; ESTROGEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOENERGY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ESTROGEN BLOOD LEVEL; FEMALE; LONGEVITY; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; SEX DIFFERENCE;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CASPASES; DNA, MITOCHONDRIAL; ENERGY METABOLISM; FEMALE; LIVER; LONGEVITY; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE, SKELETAL; MYOCARDIUM; OXIDATIVE STRESS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SEX FACTORS;

MUS;

EID: 33846379168     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2006.10.003     Document Type: Article

References (64)

1. Asdell S.A., and Joshi S.R. Reproduction and longevity in the hamster and rat. Biol. Rep. 14 (1976) 478-480
2. Asuncion J.G., Millan A., Pla R., Bruseghini L., Esteras A., Pallardo F.V., Sastre J., and Vina J. Mitochondrial glutathione oxidation correlates with age-associated oxidative damage to mitochondrial DNA. FASEB J. 10 (1996) 333-338
3. Baba T., Shimizu T., Suzuki Y., Ogawara M., Isono K., Koseki H., Kurosawa H., and Shirasawa T. Estrogen, insulin, and dietary signals to enhance resistance to oxidative stress in mice. J. Biol. Chem. 280 (2005) 16417-16426
4. Barja G. Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3 organ specificity, and relation to aging and longevity. J. Bioenerg. Biomembr. 31 (1999) 347-366
5. Barja G., and Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J. 14 (2000) 312-318
6. Barja G. Free radicals and aging. Trends Neurosci. 27 (2004) 595-600
7. Bettini E., and Maggi A. Estrogen induction of cytochrome c oxidase subunit III in rat hippocampus. J. Neurochem. 58 (1992) 1923-1929
8. Borras C., Sastre J., Garcia-Sala D., Lloret A., Pallardo F.V., and Vina J. Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic. Biol. Med. 34 (2003) 546-552
9. Borras C., Gambini J., Gomez-Cabrera M.C., Sastre J., Pallardo F.V., Mann G.E., and Vina J. 17beta-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the EKR1 and EKR2[MAPK]NFkappa B cascade. Aging Cell 4 (2005) 113-118
10. Brand M.D., Buckhinham J.A., Esteves T.C., Green K., Lambert A.J., Miwa S., Murphy M.P., Pakay J.L., Talbot D.A., and Echtay K.S. Mitochondrial superoxide and aging: uncoupling-protein activity and superoxide production. Biochem. Soc. Symp. 71 (2004) 203-213
11. Boddaert J., Mallat Z., Fornes P., Esposito B., Lecomte D., Verny M., Tedgui A., and Belmin J. Age and gender effects on apoptosis in the human coronary arterial wall. Mech. Ageing Dev. 126 (2005) 678-684
12. Carranza J., Alarcos S., Sánchez-Prieto C.B., Valencia J., and Mateos C. Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432 (2004) 215-218
13. Chen J., Delannoy M., Odwin S., He P., Trush M.A., and Yager J.D. Enhanced mitochondrial gene transcript, ATP, bcl-2 protein levels, and altered glutathione distribution in ethinyl estradiol-treated cultured female rat hepatocytes. Toxicol. Sci. 75 (1998) 271-278
14. Chen J., Li Y., Lavigne J.A., Trush M.A., and Yager J.D. Increased mitochondrial superoxide production in rat liver mitochondria, rat hepatocytes, and HepG2 cells following ethynyl estradiol treatment. Toxicol. Sci. 51 (1999) 224-235
15. Chen J., Gokhale M., Schofield B., Odwin S., and Yager J.D. Inhibition of TGF-beta-induced apoptosis by ethinyl estradiol in cultured, precision cut rat liver slices and hepatocytes. Carcinogenesis 21 (2000) 1205-1211
16. Chen J.Q., and Yager J.D. Estrogen's effects on mitochondrial gene expression: mechanisms and potential contributions to estrogens carcinogenesis. Ann. NY. Acad. Sci. 1028 (2004) 258-272
17. Chen J.Q., Yager J.D., and Russo J. Regulation of mitochondrial respiratory chain structure and function by estrogens/estrogen receptors and potential physiological/pathophysiological implications. Bioch. Biophys. Acta 1746 (2005) 1-17
18. Coto-Montes A., Tomas-Zapico C., Rodriguez-Colunga M.J., Tolivia-Cadrecha D., Martinez-Fraga J., Hardeland R., and Tolivia D. Effects of the circadian mutation 'tau' on the Harderian glands of Syrian hamsters. J. Cell Biochem. 83 (2001) 426-434
19. Cousins S.W., Marin-Castaño M.E., Espinosa-Heidmann D.G., Alexandridou A., Striker L., and Elliot S. Female gender, estrogen loss, and sub-RPE deposit formation in aged mice. IOVS 44 (2003) 1221-1229
20. Drew B., and Leeuwenburgh C. Method for measuring ATP production in brain and liver mitochondria of Fischer-344 rats with age and caloric restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285 (2003) R1259-R1267
21. Dirks A., and Leeuwenburgh C. Apoptosis in skeletal muscle with aging. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 282 (2002) R519-R527
22. Fernandez-Ballesteros R., Diez-Nicolas J., and Ruiz-Torres A. Spain. In: Schroots J., Fernandez-Ballesteros R., and Rudigner E. (Eds). Aging in Europe (1999), IOS Press, Amsterdam 107-121
23. Grossman A., Oppenheim J., Grondin G., Jean P.S., and Beaudoin A.R. Immunocytochemical localization of the [3h]estradiol-binding protein in rat pancreatic acinar cell. Endocrinology 124 (1989) 2857-2866
24. Gurwitz J.H. The age/gender interface in geriatric pharmacotherapy. J. Womens Health (Larchmt) 14 (2005) 68-72
25. Humphries S., and Stevens D.J. Out with a bang. Nature 410 (2001) 758-759
26. Herndon J.G., Tigges J., Anderson D.C., Klumpp S.A., and McClure H.M. Brain weight throughout the life span of the chimpanzee. J. Comp. Neurol. 409 (1999) 567-572
27. Hofer T., and Moller L. Reduction of oxidation during the preparation of DNA and analysis of 8-hydroxy-2′-deoxyguanosine. Chem. Res. Toxicol. 11 (1998) 882-887
28. Hofer T., Seo A.Y., Prudencio M., and Leeuwenburgh C. Method to determine RNA and DNA oxidation by HPLC-ECD; greater RNA than DNA oxidation in rat liver from doxorubicin administration. Biol. Chem. 378 (2006) 103-111
29. Justo R., Fronter M., Pujol E., Rodriguez-Cuenca S., Llado F.J., Garcia-Palmer P., Roca M., and Gianotti M. Gender-related differences in morphology and thermogenic capacity of brown adipose tissue mitochondrial subpopulations. Life Sci. 76 (2005) 1147-1158
30. Jang Y.M., Kendaia S., Drew B., Phillips T., Selman C., Julian D., and Leeuwenburgh C. Doxorubicin treatment in vivo activates caspase-12 mediated cardiac apoptosis in both male and female rats. FEBS Lett. 577 (2004) 483-490
31. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlegemuth S.E., Hofer T., Seo A.Y., Sullivan R., Jobling W.A., Morrow J.D., Van Remmen H., Sedivy J.M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., and Prolla T. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309 (2005) 481-484
32. Latorre A., Moya A., and Ayala A. Evolution of mitochondrial DNA in Drosophila suboscura. Proc. Natl. Acad. Sci. USA 83 (1986) 8649-8653
33. Mallat Z., Fornes P., Costagliola R., Esposito B., Belmin J., Lecomte D., and Tedgui A. Age and gender effects on cardiomyocyte apoptosis in the normal human heart. J. Gerontol. A Biol. Sci. Med. Sci. 56 (2001) M719-M723
34. McCulloch D., and Gems D. Evolution of male longevity bias in nematodes. Aging Cell 2 (2003) 165-173
35. Mela L., and Seitz S. Isolation of mitochondria with emphasis on heart mitochondria from small amounts of tissue. Methods Enzymol. 55 (1979) 39-46
36. Monje P., Zanello S., Holick M., and Boland R. Differential cellular localization of estrogen receptor alpha in uterine and mammary cells. Mol. Cell Endocrinol. 181 (2001) 117-129
37. Pamplona R., Portero-Otin M., Riba D., Requena J.R., Thorpe S.R., Lopez-Torres M., and Barja G. Low fatty acid unsaturation: a mechanism for lowered lipoperoxidative modification of tissue proteins in mammalian species with long life span. J. Gerontol. A Biol. Sci. Med. Sci. 55 (2000) B286-B291
38. Pansarasa O., Castagna L., Colombi B., Vecchiet J., Felzani G., and Marzatico F. Age and sex differences in human skeletal muscle: role of reactive oxygen species. Free Radic. Res. 33 (2000) 287-293
39. Pedram A., Razandi M., Wallace D.C., and Levin E.R. Functional estrogen receptors in the mitochondria of breast cancer cells. Mol. Biol. Cell 17 (2006) 2125-2137
40. Pollack M., and Leeuwenburgh C. Apoptosis and aging: role of the mitochondria. J. Gerontol. A Biol. Sci. Med. Sci. 56 (2001) B475-B482
41. Rodriguez-Cuenca S., Pujol E., Justo R., Frontera M., Oliver J., Gianotti M., and Roca P. Sex-dependent thermogenesis differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J. Biol. Chem. 45 (2002) 42958-42963
42. Rollo C.D. Growth negatively impacts the life span of mammals. Evol. Dev. 4 (2002) 55-61
43. Rowlatt C., Chesterman F.C., and Sheriff M.U. Lifespan, age changes and tumour incidence in an ageing C57BL mouse colony. Lab. Anim. 10 (1976) 419-442
44. Sanz A., Caro P., and Barja G. Protein restriction without strong caloric restriction decreases mitochondrial oxygen radical production and oxidative DNA damage in rat liver. J. Bioenerg. Biomembr. 36 (2004) 542-552
45. Sanz A., Caro P., Ibanez J., Gomez J., Gredilla R., and Barja G. Dietary restriction at old age lowers mitochondrial oxygen radical production and leak at complex I and oxidative DNA damage in rat brain. J. Bioenerg. Biomembr. 37 (2005) 83-90
46. Sanz A., Gredilla R., Pamplona R., Portero-Otin M., Vara E., Tresguerres J.A., and Barja G. Effect of insulin and growth hormone on rat heart and liver oxidative stress in control and caloric restricted animals. Biogerontology 6 (2005) 15-26
47. Sanz A., Caro P., Ayala V., Portero-Otín M., Pamplona R., and Barja G. Methionine restriction decreases mitochondrial oxygen radical generation and leak and oxidative damage to mitochondrial DNA and proteins. FASEB J. 20 (2006) 1064-1073
48. Sanz A., Pamplona R., and Barja G. Is the mitochondrial free radical theory of aging intact?. Antioxid. Redox Signal. 8 (2006) 582-599
49. Sanz A., and Barja G. Estimation of the rate of production of oxygen radicals at mitochondria. In: Conn M. (Ed). Handbook of Models for the Study of Human Aging 16 (2006), Academic Press 183-189
50. Seo A.Y., Hofer T., Sung B., Judge S., Chung H.Y., and Leeuwenburgh C. Hepatic oxidative stress during aging: effects of 8% long-term calorie restriction and lifelong exercise. Antioxid. Redox Signal. 8 (2006) 529-538
51. Shelke R., and Leeuwenburgh C. Life-long calorie restriction (CR) increases expression of apoptosis repressor with a caspase recruitment domain (ARC) in the brain. FASEB J. 17 (2003) 494-496
52. Smith D.W. Is greater female's longevity a general finding among animals?. Biol. Rev. Camb. Physiol. Soc. 64 (1989) 1-12
53. Sohal R.S., Svensson I., Sohal B.H., and Brunk U.T. Superoxide anion radical production in different animal species. Mech. Ageing Dev. 49 (1989) 129-135
54. Speakman J.R. Body size, energy metabolism and lifespan. J. Exp. Biol. 208 (2005) 1717-1730
55. Sverko V., Balog T., Sovocanec S., Gavella M., and Marotti T. Age-associated alteration of lipid peroxidation and superoxide dismutase activity in CBA and AKR mice. Exp. Gerontol. 37 (2002) 1031-1039
56. Sverko V., Sobocanec S., Balog T., and Marotti T. Age and gender differences in antioxidant enzyme activity: potential relationship to liver carcinogenesis in mice. Biogerontology 5 (2004) 235-242
57. Tanaka S., Segawa T., Tamaya N., and Ohno T. Establishment of an aging farm of F344:N rats and C57BL/6 mice at the national institute for longevity sciences (NILS). Arch. Gerontol. Geriatr. 30 (2000) 215-223
58. Taylor E.R., Hurrell F., Shannon R.J., Lin T.K., Hirst J., and Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 278 (2003) 19603-19610
59. Valle A., Catala-Niell B., Colom F.J., Garcia-Palmer F.J., Oliver J., and Roca P. Sex-related differences in energy balance in response to caloric restriction. Am. J. Physiol. Endocrinol. Metab. 289 (2005) E15-E22
60. Vina J., Borras C., Gambini J., Sastre J., and Pallardo F.V. Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds. FEBS Lett. 579 (2005) 2541-2545
61. Wang H., Liu H., and Liu R. Gender difference in glutathione metabolism during aging in mice. Exp. Gerontol. 38 (2003) 507-517
62. Weisz A., Basile W., Scafoglio L., Altucci F., Bresciani A., Facchiano A., Sismondi L., Cicatiello M., and De Bortoli M. Molecular identification of eralpha-positive breast cancer cells by the expression of profile of an intrinsic set of estrogen regulated genes. J. Cell Physiol. 200 (2004) 440-450
63. Which S.A., Utami-Atmoko S.S., Setia T.M., Rijksen H.D., Schurmann C., van Hooff J.A.R.A.M., and van Schaik C.P. Life story of wild Sumatran orangutans (Pongo abelii). J. Human Evol. 47 (2004) 385-398
64. Yunis E.J., Watson A.L.M., Gelman R., Sylvia S.J., Bronson R., and Dorf M.E. Traits that influence longevity in mice. Genetics 108 (1984) 999-1011