Poor maternal nutrition followed by accelerated postnatal growth leads to alterations in DNA damage and repair, oxidative and nitrosative stress, and oxidative defense capacity in rat heart

FASEB Journal

Volumn 27, Issue 1, 2013, Pages 379-390

  Tarry Adkins, Jane L ^a   Martin Gronert, Malgorzata S ^a   Fernandez Twinn, Denise S ^a   Hargreaves, Iain ^b   Alfaradhi, Maria Z ^a   Land, John M ^b   Aiken, Catherine E ^a   Ozanne, Susan E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Aging; Cardiovascular disease; Developmental programming

Indexed keywords

3 NITROTYROSINE; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; DNA GLYCOSYLTRANSFERASE; ENDONUCLEASE; HEME OXYGENASE 1; MANGANESE SUPEROXIDE DISMUTASE; PEROXIREDOXIN 3; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE; XRCC1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL AGING; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; FEMALE; GENE EXPRESSION; GROWTH ACCELERATION; HEART; HEART WEIGHT; LACTATION; LOW BIRTH WEIGHT; MALE; MATERNAL NUTRITION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; POSTNATAL GROWTH; PRIORITY JOURNAL; PROGENY; RAT; SINGLE STRANDED DNA BREAK; WEANING;

ANIMALS; BASE SEQUENCE; BODY WEIGHT; DNA DAMAGE; DNA PRIMERS; DNA REPAIR; DNA, MITOCHONDRIAL; FEMALE; GENE EXPRESSION PROFILING; GROWTH; MALNUTRITION; MYOCARDIUM; NITROSATION; ORGAN SIZE; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, WISTAR; TELOMERE;

ANIMALIA; RATTUS;

EID: 84871910435     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-218685     Document Type: Article

References (56)

1. Barker, D. J. P., Winters, P. D., Osmond, C., Margetts, B., and Simmonds, S. J. (1989) Weight in infancy and death from ischaemic heart disease. Lancet 334, 577-580 (Pubitemid 19216205)
2. Barker, D. J. P., Bull, A. R., Osmond, C., and Simmonds, S. J. (1990) Fetal and placental size and risk of hypertension in adult life. BMJ 301, 259-262 (Pubitemid 20241224)
3. Barker, D. J. P., Gluckman, P. D., Godfrey, K. M., Harding, J. E., Owens, J. A., and Robinson, J. S. (1993) Fetal Nutrition and cardiovascular disease in adult life. Lancet 341, 938-941 (Pubitemid 23109122)
4. Leeson, C. P. M., Kattenhorn, M., Morley, R., Lucas, A., and Deanfield, J. E. (2001) Impact of low birth weight and cardiovascular risk factors on endothelial function in early adult life. Circulation 103, 1264-1268 (Pubitemid 32221350)
5. Hales, C. N., and Barker, D. J. P. (2001) The thrifty phenotype hypothesis. Br. Med. Bull. 60, 5-20 (Pubitemid 34123501)
6. Eriksson, J. G., Forsen, T., Tuomilehto, J., Osmond, C., and Barker, D. (2000) Fetal and childhood growth and hypertension in later life. Hypertension 36, 790-794
7. Eriksson, J. G., Forsen, T., Tuomilehto, J., Winter, P. D., Osmond, C., and Barker, D. (1999) Catch up growth in childhood and death from coronary heart disease: longitudinal study. BMJ 318, 427-431 (Pubitemid 29192114)
8. Singhal, A., Cole, T. J., Fewtrell, M., Deanfield, J., and Lucas, A. (2004) Is slower early growth beneficial for long term cardiovascular health? Circulation 109, 1108-1113 (Pubitemid 38332614)
9. Godfrey, K. M., Inskip, H. M., and Hanson, M. A. (2011) The long term effects of prenatal development on growth and metabolism. Semin. Reprod. Med. 29, 257-265
10. Corstius, H. B., Zimanyi, M. A., Maka, N., Herath, T., Thomas, W., Van Der Laarse, A., Wreford, N. G., and Black, M. J. (2005) Effect of intrauterine growth restriction on the number of cardimyocytes in rat hearts. Pediatr. Res. 57, 796-800 (Pubitemid 40727108)
11. Skilton, M. R., Gosby, A. K., Wu, B. J., Ho, L. M. L., Stocker, R., Caterson, I. D., and Celermajer, D. S. (2006) Maternal undernutrition reduces aortic wall thickness and elastin content in offspring of rats without altering endothelial function. Clin. Sci. (Lond.) 111, 281-287 (Pubitemid 44599875)
12. Lim, K., Zimanyi, M. A., and Black, M. J. (2006) Effect of maternal protein restriction on rats on cardiac fibrosis and capilliarization in adulthood. Pediatr. Res. 60, 83-87 (Pubitemid 44297618)
13. Jennings, B. J., Ozanne, S. E., Dorling, M. W., and Hales, C. N. (1999) Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett. 448, 4-8
14. Ozanne, S. E., and Hales, C. N. (2004) Lifespan: catch-up growth and obesity in male mice. Nature 427, 411-412 (Pubitemid 38168484)
15. Haussman, M. F., Winkler, D. W., O'Reilly, K. M., Huntingdon, C. E., Nisbet, I. C., and Vleck, C. M. (2003) Telomeres shorten more slowly in long-lived bird and mammals than in short-lived ones. Proc. Biol. Sci. 270, 1387-1392 (Pubitemid 36831300)
16. Jemielity, S., Kimura, M., Parker, K. M., Parker, X. D., Cao, X., Aviv, A., and Keller, L. (2007) Short telomeres in short-lived males: what are the molecular and evolutionary causes? Aging Cell 2, 225-233 (Pubitemid 46455066)
17. Tarry-Adkins, J. L., Martin-Gronert, M. S., Chen, J. H., Cripps, R. L., and Ozanne, S. E. (2008) Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J. 22, 2037-2044 (Pubitemid 351811479)
18. Shelley, P., Tarry-Adkins, J., Martin-Gronert, M. S., Poston, L., Heales, S., Clark, J., Ozanne, S., and McConnell, J. (2007) Rapid neonatal weight gain in rats results in a renal ubiquinone (CoQ) deficiency associated with premature death. Mech. Ageing Dev. 128, 681-687 (Pubitemid 350299051)
19. Tarry-Adkins, J. L., Chen, J. H., Smith, N. S., Jones, R. H., Cherif, H., and Ozanne, S. E. (2009) Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cellular senescence in rat islets. FASEB J. 23, 1521-1528
20. Minamino, T., and Komuru, I. (2008) Role of telomeres in vascular senescence. Front. Biosci. 13, 2971-2979 (Pubitemid 351589213)
21. Dei Cas, A., Spigoni, V., Franzini, L., Preti, M., Ardigo, D., Derlindati, E., Metra, M., Monti, M. D., Dell'ara, P., Gnudi, L., and Zavaroni, I. (2011) Lower endothelial progenitor cell number, family history of cardiovascular disease and reduced HDL-cholesterol levels are associated with shorter leukocyte telomere length in healthy young adults.Nutr. Metab. Cardiovasc. Dis. doi: 10.1016/j.numecd.2011.04.005
22. Kawanishi, S., and Oikawa, S. (2004) Mechanism of telomere shortening by oxidative stress. Ann. N. Y. Acad. Sci. 1019, 278-284 (Pubitemid 38951320)
23. Sitte, N., Saretzki, G., and von Zglincki, T. (1998) Accelerated telomere shortening in fibroblasts after extended periods of confluency. Free Radic. Biol. Med. 24, 885-893 (Pubitemid 28186228)
24. Richter, T., and von Zglinicki, T. (2007) A continuous correlation between oxidative stress and telomere length in human fibroblasts. Exp. Gerontol. 11, 1039-1042 (Pubitemid 47633455)
25. Von Zglinicki, T., Pilger, R., and Sitte, N. (2000) Accumulation of single-strand breaks is the major cause of telomere shortening in human fibroblasts. Free Radic. Biol. Med. 28, 64-74 (Pubitemid 30045574)
26. Griendling, K. K., and Fitzgerald, G. A. (2003) Oxidative stress and cardiovascular injury. Circulation 108, 2034-2040
27. Csiszar, A., Pacher, P., Kaley, G., and Ungarvi, Z. (2005) Role of nitrosative and oxidative stress, longevity genes, and Poly(ADP-ribose) polymerase in cardiovascular dysfunction associated with aging. Curr. Vasc. Pharmacol. 3, 285-291 (Pubitemid 40933050)
28. Heistad, D. D. (2006) Oxidative stress and vascular disease. Arterioscler. Thromb. Vasc. Biol. 26, 689-695
29. Sasaki, T., Unno, K., Tahara, S., and Kaneko, T. (2010) Age-related increase of reactive oxygen generation in the brains of mammals and birds: Is reactive oxygen a signaling molecule to determine the aging process and life span? Geriatrics Gerontol. Int. 10, S10-S24
30. Salgo, M. G., Bermudez, E., Squadrito, G. L., and Pryor, W. A. (1995) DNA-damage and oxidation of thiols peroxynitrite causes in rat thymocytes (corrected) Arch Biochem. Biophys. 322, 500-505
31. Snoeck, A., Remacle, C., Reusens, B., and Hoett, J. J. (1990) Effect of low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol. Neonate 57, 107-118 (Pubitemid 20041117)
32. Tarry-Adkins, J. L., Ozanne, S. E., Norden, A., Cherif, H., and Hales, C. N. (2006) Lower antioxidant capacity and elevated p53 and p21 may be a link between gender disparity in renal telomere shortening, albuminuria, and longevity. Am. J. Physiol. Renal Physiol. 290, F509-F516
33. Nicklas, J. A., Brooks, J. M., Hunter, T. C., Single, R., and Branda, R. F. (2004) Development of a quantitative PCR (Taqman) assay for relative mitochondrial copy number and the common mitochondrial DNA deletion in rat. Environ. Mol. Mutagen. 44, 313-320 (Pubitemid 39447235)
34. Ragan C. I., Wilson M. Y., and Darley-Usman V. M. (1988) Subfractionation of mitochondria and isolation of proteins of oxidative phosphorylation. In Mitochondria: A Practical Approach. (Darley V. M., Rickwood, D, and Wilson M. T., eds) pp. 79-113, IRL Press, Oxford, UK
35. King, T. E. (1967) Preparation of succinate cytochrome c reductase and cytochrome b-c1 particle and reconstruction of Succinate cytochrome c reductase. Methods Enzymol. 10, 446-451
36. Wharton, D. C., and Tzagoloff, A. (1967) Cytochrome oxidase from beef heart mitochondria. Methods Enzymol. 10, 245-250
37. Shepherd, J. A., and Garland, P. B. (1969) Citrate synthase activity from rat liver. Methods Enzymol. 13, 11-19
38. Yamakura, F., Taka, H., Fujimura, T., and Murayama, K. (1998) Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J. Biol. Chem. 273, 14085-14089 (Pubitemid 28319114)
39. Horton, J., Watson, M., Stefanik, D. F., Shaughnessy, D. T., Taylor, J. A., and Wilson, S. H. (2008) XRCC1 and DNA polymerase β in cellular protection against cytotoxic DNA single-strand breaks. Cell Res. 18, 48-63
40. Harzra, T. K., Das, A., Das, A., Choudhury, S., Kow, Y. W., and Roy, R. (2007) Oxidative DNA damage repair in mammalian cells: A new perspective. DNA Repair (Amst.) 6, 470-480 (Pubitemid 46357682)
41. Lehrer, J. E., Firestein, B. L., and Bredt, D. S (2000) Nitric oxide mediated induction of cytochrome c mRNA and protein in a mouse macrophage cell line. Neurosci. Lett. 288, 107-110 (Pubitemid 30392422)
42. Bedard, K., and Krause, K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313 (Pubitemid 46209993)
43. Wang, M., Zhang, J., Walker, S. J., Dworakoswki R., Lakatta., E. G., and Shah, A. M. (2010) Involvement of NADPH oxidase in age-associated cardiac remodelling. J. Mol. Cell. Cardiol. 48, 762-727
44. Meischl, C., Krijnen, P. A., Sipkens, J. A., Cillessen, S. A., Munoz, I. G., Okroj, M., Ramska, M., Muller, A., Visser, C. A., Musters, R. J., Simonides, W. S., Hack, C. E., Roos, D., and Niessen, H. W. (2006) Ischemia induces nuclear NOX2 expression in cardiomyocytes and subsequently activates apoptosis. Apoptosis 11, 913-921 (Pubitemid 43876822)
45. Krijnen, P. A., Meischl, C., Hack, C. E., Meijer, C. J., Visser, C. A., Roos, D., and Niessen, H. W. (2003) Increased NOX2 expression in human cardiomyocytes after myocardial infarction. J. Clin. Pathol. 56, 194-199 (Pubitemid 36308034)
46. Kim, Y. M., Guzik, T. J., Zhang, Y. H., Zhang, M. H., Kattach, H., Ratnatunga, C., Pillai, R., Channon, K. M., and Casadel, B. (2003) A myocardial NOX2 containing NAD(P)H oxidase contributes to oxidative stress in human atrial fibrillation. Circ. Res. 97, 629-636 (Pubitemid 41416331)
47. Kuroda, J., Ago, T., Matsushima, S., Zhai, P., Schneider, M., and Sadoshima, J. (2010) NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc. Natl. Acad. Sci. U. S. A. 107, 15565-15570
48. Ago, T., Matsushima, S., Kuroda, J., Zablocki, D., Kitazono, T., and Sadoshima, J. (2010) The NADPH Oxidase Nox4 and aging in the heart. Aging 2, 1012-1016
49. Sindhu, R. K., Roberts, C. K., Ehdaie, A., Zhan, C., and Vaziri, N. D. (2005) Effects of aortic coarctation on aortic antioxidant enzymes and NADPH oxidase protein expression. Life Sci. 76, 945-953 (Pubitemid 39601897)
50. MacMillan-Crow, L. A., Crow, J. P., and Thompson, J. A. (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37, 1613-1622 (Pubitemid 28093677)
51. Alvarez, B., Deronica, R., Duran, R., and Trujillo, C. (2004) Inactivation of human Cu, Zn superoxide dismutase by peroxynitrite and histinyl radical. Free. Radic. Biol. Med. 37, 813-822 (Pubitemid 39078553)
52. Son, E., Jeong, J., Lee, J., Jung, D. Y., Cho, G. J., Choi, W. S., Lee, M. S., Kim, S. H., Kim, I. K., and Suk, K. (2005) Sequential induction of heme-oxygenase I and manganese superoxide dismutase protects cultured astrocytes against nitric oxide. Biochem. Pharm. 70, 590-597 (Pubitemid 40978549)
53. Li, L., Shoji, W., Takano, H., Nishimura, N., Aoki, Y., Takahashi, R., Goto, S., Kaifu, T., Takai, T., and Obinata, M. (2007) Increased susceptibility of MER5 (peroxiredoxin III) knockout mice to LPS-induced oxidative stress. Biochem. Biophys. Res. Commun. 13, 715-721 (Pubitemid 46330210)
54. Li, L., Kaifu, T., Obinata, M., and Takai, T. (2009) Peroxiredoxin III-deficiency sensitizes macrophages to oxidative stress. J. Biochem. 145, 425-427
55. Sen, S., and Simmons, R. A. (2010) Maternal antioxidant supplementation prevents adiposity in Western diet fed rats. Diabetes 59, 3058-3065
56. Thakor, A. S., Richter, H. G., Kane, A. D., Dunster, C. A., Kelly, F. J., Poston, L., and Giussani, D. A (2010) Redox modulation of the fetal cardiovascular defence to hypoxaemia. J. Physiol. 588, 4235-4247