Maternal protein restriction affects gene expression profiles in the kidney at weaning with implications for the regulation of renal function and lifespan

Clinical Science

Volumn 119, Issue 9, 2010, Pages 373-384

  Chen, Jian Hua ^a   Tarry Adkins, Jane L ^a   Matharu, Kieran ^a   Yeo, Giles S H ^a   Ozanne, Susan E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Developmental programming; Lifespan; Maternal diet; Renal function; Senescence; Stress response

Indexed keywords

ALBUMIN; ALPHA SYNUCLEIN; ANGIOPOIETIN 1; ANKYRIN; ANKYRIN 2; BETA6 INTEGRIN; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE 14; CARBOXYLESTERASE; CARBOXYLESTERASE 3; CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; DIHYDROPYRIMIDINE DEHYDROGENASE; DUAL SPECIFICITY PHOSPHATASE 6; GELATINASE A; GLYCINE DEHYDROGENASE (DECARBOXYLATING); HEME OXYGENASE 1; KLOTHO PROTEIN; LON PEPTIDASE 2; NUAK ENZYME; PEPTIDASE; PHOSPHOTRANSFERASE; PROTOPORPHYRINOGEN OXIDASE; RAD52 PROTEIN; RING FINGER PROTEIN; RING FINGER PROTEIN 12; SESTRIN 1; TRANSCRIPTION FACTOR FKHRL1; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; VITAMIN D; PROTEIN INTAKE;

AGED; ALBUMINURIA; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CELL PROTECTION; CONTROLLED STUDY; DOWN REGULATION; ENZYME REGULATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; HOMEOSTASIS; KIDNEY FUNCTION; KIDNEY MASS; LACTATION; LIFESPAN; LONGEVITY; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN RESTRICTION; SENESCENCE; UPREGULATION; ADMINISTRATION AND DOSAGE; AGING; ANATOMY AND HISTOLOGY; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; MATERNAL NUTRITION; METABOLISM; ORGAN SIZE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PROTEIN INTAKE; URINE; WEANING;

AGING; ALBUMINURIA; ANIMALS; BODY WEIGHT; DIETARY PROTEINS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; KIDNEY; LONGEVITY; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE; MICE, INBRED C57BL; ORGAN SIZE; WEANING;

EID: 77956379045     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20100230     Document Type: Article

References (58)

1. Beckman, K. B. and Ames, B. N. (1998) The free radical theory of aging matures. Physiol. Rev. 78, 547-581
2. Muller, F. L., Lustgarten, M. S., Jang, Y., Richardson, A. and Van Remmen, H. (2007) Trends in oxidative aging theories. Free Radical Biol. Med. 43, 477-503
3. Vina., J., Borras, C. and Miquel, J. (2007) Theories of ageing. IUBMB Life 59, 249-254
4. Kenyon, C. (2005) The plasticity of aging: insights from long-lived mutants. Cell 120, 449-460
5. Hekimi, S. (2006) How genetic analysis tests theories of animal aging. Nat. Genet. 38, 985-991
6. Ladiges, W., Van Remmen, H., Strong, R., Ikeno, Y., Treuting, P., Rabinovitch, P. and Richardson, A. (2009) Lifespan extension in genetically modified mice. Aging Cell 8, 346-352
7. Partridge, L. and Gems, D. (2002) Mechanisms of ageing: public or private? Nat. Rev. Genet. 3, 165-175
8. Russell, S. J. and Kahn, C. R. (2007) Endocrine regulation of ageing. Nat. Rev. Mol. Cell Biol. 8, 681-691
9. Berryman, D. E., Christiansen, J. S., Johannsson, G., Thorner, M. O. and Kopchick, J. J (2008) Role of the GH/IGF-1 axis in lifespan and healthspan: Lessons from animal models. Growth Horm. IGF Res. 18, 455-471
10. Kenyon, C., Chang, J., Gensch, E., Rudner, A. and Tabtiang, R. (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366, 461-464 (Pubitemid 24013878)
11. Giannakou, M. E. and Partridge, L. (2007) Role of insulin-like signalling in Drosophila lifespan. Trends Biochem. Sci. 32, 180-188
12. Bartke, A. (2005) Minireview: role of the growth hormone/insulin-like growth factor system in mammalian aging. Endocrinology 146, 3718-3723 (Pubitemid 41175738)
13. Bartke, A. (2008) Insulin and aging. Cell Cycle 7, 3338-3343
14. Lee, C. K., Klopp, R. G., Weindruch, R. and Prolla, T. A. (1999) Gene expression profile of aging and its retardation by caloric restriction. Science 285, 1390-1393
15. Lee, C. K., Weindruch, R. and Prolla, T. A. (2000) Gene-expression profile of the ageing brain in mice. Nat. Genet. 25, 294-297
16. Park, S. K. and Prolla, T. A. (2005) Lessons learned from gene expression profile studies of aging and caloric restriction. Ageing Res. Rev. 4, 55-65
17. Lustig, A., Weeraratna, A. T.,Wood, III, W.W., Teichberg, D., Bertak, D., Carter, A., Poosala, S., Firman, J., Becker, K. G., Zonderman, A. B. et al. (2007) Transcriptome analysis of age-, gender- and diet-associated changes in murine thymus. Cell. Immunol. 245, 42-61
18. Park, S. K., Kim, K., Page, G. P., Allison, D. B.,Weindruch, R. and Prolla, T. A. (2009) Gene expression profiling of aging in multiple mouse strains: identification of aging biomarkers and impact of dietary antioxidants. Aging Cell 8, 484-495
19. Zahn, J. M., Poosala, S., Owen, A. B., Ingram, D. K., Lustig, A., Carter, A., Weeraratna, A. T., Taub, D. D., Gorospe, M., Mazan-Mamczarz, K. et al. (2007) AGEMAP: a gene expression database for aging in mice. PLoS Genet 3, e201
20. Kim, S. K. (2007) Common aging pathways in worms, flies, mice and humans. J. Exp. Biol. 210, 1607-1612
21. 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
22. Ozanne, S. E. and Hales, C. N. (2004) Lifespan: catch-up growth and obesity in male mice. Nature 427, 411-412
23. Chen, J. H., Martin-Gronert, M. S., Tarry-Adkins, J. and Ozanne, S. E. (2009) Maternal protein restriction affects postnatal growth and the expression of key proteins involved in lifespan regulation in mice. PLoS ONE 4, e4950
24. Chen, J. H., Tarry-Adkins, J. L., Heppolette, C. A., Palmer, D. B. and Ozanne, S. E. (2010) Early-life nutrition influences thymic growth in male mice that may be related to the regulation of longevity. Clin. Sci. 118, 429-438
25. Martin, J. E. and Sheaff, M. T. (2007) Renal ageing. J. Pathol. 211, 198-205
26. Harris, R. C. and Neilson, E. G. (2006) Toward a unified theory of renal progression. Annu. Rev. Med. 57, 365-380
27. Percy, C. J., Power, D. and Gobe, G. C. (2008) Renal ageing: changes in the cellular mechanism of energy metabolism and oxidant handling. Nephrology 13, 147-152
28. Kurosu, H., Yamamoto, M., Clark, J. D., Pastor, J. V., Nandi, A., Gurnani, P., McGuinness, O. P., Chikuda, H., Yamaguchi, M., Kawaguchi, H. et al. (2005) Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833
29. Lustig, A., Carter, A., Bertak, D., Enika, D., Vandanmagsar, B., Wood, W., Becker, K. G., Weeraratna, A. T. and Taub, D. D. (2009) Transcriptome analysis of murine thymocytes reveals age-associated changes in thymic gene expression. Int. J. Med. Sci. 6, 51-64
30. Kuro-o, M. (2009) Klotho and aging. Biochim. Biophys. Acta 1790, 1049-1058
31. Razzaque, M. S. (2007) Does renal ageing affect survival? Ageing Res. Rev. 6, 211-222
32. Hong, C. Y. and Chia, K. S. (1998) Markers of diabetic nephropathy. J. Diabetes Complications 12, 43-60
33. Birn, H. and Christensen, E. I. (2006) Renal albumin absorption in physiology and pathology. Kidney Int. 69, 440-449
34. Hoppe, C. C., Evans, R. G., Bertram, J. F. and Moritz, K. M. (2007) Effects of dietary protein restriction on nephron number in the mouse. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1768-R1774
35. Moritz, K. M., Dodic, M. and Wintour, E. M. (2003) Kidney development and the fetal programming of adult disease. BioEssays 25, 212-220
36. Rodwell, G. E., Sonu, R., Zahn, J. M., Lund, J.,Wilhelmy, J., Wang, L., Xiao, W., Mindrinos, M., Crane, E., Segal, E. et al. (2004) A transcriptional profile of aging in the human kidney. PLoS Biol. 2, e427 (Pubitemid 40280523)
37. Galbraith, R. (1999) Heme oxygenase: who needs it? Proc. Soc. Exp. Biol. Med. 222, 299-305
38. Courtney, A. E. and Maxwell, A. P. (2008) Heme oxygenase 1: does it have a role in renal cytoprotection? Am. J. Kidney. Dis. 51, 678-690
39. Pileggi, A., Molano, R. D., Berney, T., Cattan, P., Vizzardelli, C., Oliver, R., Fraker, C., Ricordi, C., Pastori, R. L., Bach, F. H. and Inverardi, L. (2001) Heme oxygenase-1 induction in islet cells results in protection from apoptosis and improved in vivo function after transplantation. Diabetes 50, 1983-1991 (Pubitemid 33643664)
40. Chen, Y. S., Zhu, X. X., Zhao, X. Y., Xing, H. Y. and Li, Y. G. (2008) Hemin, a heme oxygenase-1 inducer, improves aortic endothelial dysfunction in insulin resistant rats. Chin. Med. J. 121, 241-247
41. Wasserberg, N., Pileggi, A., Salgar, S. K., Ruiz, P., Ricordi, C., Inverardi, L. and Tzakis, A. G. (2007) Heme oxygenase-1 upregulation protects against intestinal ischemia/reperfusion injury: a laboratory based study. Int. J. Surg. 5, 216-224
42. Abraham, N. G., Cao, J., Sacerdoti, D., Li, X. and Drummond, G. (2009) Heme oxygenase: the key to renal function regulation. Am. J. Physiol. Renal Physiol. 297, F1137-F1152
43. Jarmi, T. and Agarwal, A. (2009) Heme oxygenase and renal disease. Curr. Hypertens. Rep. 11, 56-62
44. Rattan, S. I. (2008) Hormesis in aging. Ageing Res. Rev. 7, 63-78
45. Tarry-Adkins, J. L., Joles, J. A., Chen, J. H., Martin-Gronert, M. S., van der Giezen, D. M., Goldschmeding, R., Hales, C. N. and Ozanne, S. E. (2007) Protein restriction in lactation confers nephroprotective effects in the male rat and is associated with increased anti-oxidant expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1259-R1266
46. Lefebvre, D. L., Bai, Y., Shahmolky, N., Sharma, M., Poon, R., Drucker, D. J. and Rosen, C. F. (2001) Identification and characterization of a novel sucrose-non-fermenting protein kinase/AMP-activated protein kinase-related protein kinase, SNARK. Biochem. J. 355, 297-305 (Pubitemid 32397787)
47. Lefebvre, D. L. and Rosen, C. F. (2005) Regulation of SNARK activity in response to cellular stresses. Biochim. Biophys. Acta 1724, 71-85
48. Humbert, N., Navaratnam, N., Augert, A., Da Costa, M., Martien, S., Wang, J., Martinez, D., Abbadie, C., Carling, D., de Launoit, Y. et al. (2010) Regulation of ploidy and senescence by the AMPK-related kinase NUAK1. EMBO J. 29, 376-386
49. 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 cell senescence in rat islets. FASEB J. 23, 1521-1528
50. Yoshida, T., Fujimori, T. and Nabeshima, Y. (2002) Mediation of unusually high concentrations of 1,25-dihydroxyvitamin D in homozygous klotho mutant mice by increased expression of renal 1α-hydroxylase gene. Endocrinology 143, 683-689
51. Ohnishi, M., Nakatani, T., Lanske, B. and Razzaque, M. S. (2009) Reversal of mineral ion homeostasis and soft-tissue calcification of klotho knockout mice by deletion of vitamin D 1α-hydroxylase. Kidney Int. 75, 1166-1172
52. Petropoulos, I. and Friguet, B. (2006) Maintenance of proteins and aging: the role of oxidized protein repair. Free Radical Res. 40, 1269-1276 (Pubitemid 44698276)
53. Ngo, J. K. and Davies, K. J. (2007) Importance of the lon protease in mitochondrial maintenance and the significance of declining lon in aging. Ann. N.Y. Acad. Sci. 1119, 78-87
54. Daitoku, H. and Fukamizu, A. (2007) FOXO transcription factors in the regulatory networks of longevity. J. Biochem. 141, 769-774 (Pubitemid 351455333)
55. Sedding, D. G. (2008) FoxO transcription factors in oxidative stress response and ageing: a new fork on the way to longevity? Biol. Chem. 389, 279-283
56. Budanov, A. V., Sablina, A. A., Feinstein, E., Koonin, E. V. and Chumakov, P. M. (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304, 596-600
57. Kopnin, P. B., Agapova, L. S., Kopnin, B. P. and Chumakov, P. M. (2007) Repression of sestrin family genes contributes to oncogenic Ras-induced reactive oxygen species up-regulation and genetic instability. Cancer Res. 67, 4671-4678
58. Lee, J. H., Budanov, A. V., Park, E. J., Birse, R., Kim, T. E., Perkins, G. A., Ocorr, K., Ellisman, M. H., Bodmer, R., Bier, E. and Karin, M. (2010) Sestrin as a feedback inhibitor of TOR that prevents age-related pathologies. Science 327, 1223-1228