Short-term calorie restriction protects against renal senescence of aged rats by increasing autophagic activity and reducing oxidative damage

Mechanisms of Ageing and Development

Volumn 134, Issue 11-12, 2013, Pages 570-579

  Ning, Yi Chun ^a,b   Cai, Guang Yan ^a   Zhuo, Li ^a   Gao, Jian Jun ^a   Dong, Dan ^a   Cui, Shaoyuan ^a   Feng, Zhe ^a   Shi, Suo Zhu ^a   Bai, Xue Yuan ^a   Sun, Xue Feng ^a   Chen, Xiang Mei ^a,b  

^a CHINESE PLA GENERAL HOSPITAL   (China)

^b NANKAI UNIVERSITY   (China)

Author keywords

Aging; Autophagy; Calorie restriction; Kidney; Oxidative damage

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; CREATININE; HISTONE DEACETYLASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL DNA; PROTEIN; SIRTUIN 1; TRIACYLGLYCEROL;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BODY WEIGHT; CALORIC RESTRICTION; CHEMOLUMINESCENCE; DENSITOMETRY; FOOD INTAKE; GLOMERULUS FILTRATION RATE; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; MALE; MORPHOLOGY; NONHUMAN; ORGAN SIZE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN URINE LEVEL; QUANTITATIVE ANALYSIS; RAT; SENESCENCE; SEQUENCE HOMOLOGY; TRIACYLGLYCEROL BLOOD LEVEL; UBIQUITINATION;

RATTUS;

8-HYDROXYDEOXYGUANOSINE; 8-OHDG; AD LIBITUM; AGING; AL; AMP-ACTIVATED PROTEIN KINASE; AMPK; AUTOPHAGY; CALORIE RESTRICTION; CHRONIC KIDNEY DISEASE; CKD; CR; KIDNEY; MITOCHONDRIAL DNA; MTDNA; O; OLD; OXIDATIVE DAMAGE; PAS; PERIODIC ACID-SCHIFF; SA-Β-GAL; SDRS; SENESCENCE-ASSOCIATED Β-GALACTOSIDASE; SPRAGUE-DAWLEY RATS; Y; YOUNG;

ADENOSINE MONOPHOSPHATE; AGE FACTORS; AGING; ANIMALS; AUTOPHAGY; BETA-GALACTOSIDASE; BODY WEIGHT; CALORIC RESTRICTION; CELL AGING; DEOXYGUANOSINE; DNA, MITOCHONDRIAL; FIBROSIS; GENE EXPRESSION PROFILING; KIDNEY; MALE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SIRTUIN 1; TOR SERINE-THREONINE KINASES;

EID: 84891558933     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2013.11.006     Document Type: Article

References (56)

1. Anderson S., Halter J.B., Hazzard W.R., Himmelfarb J., Horne F.M., Kaysen G.A., Kusek J.W., Nayfield S.G., Schmader K., Tian Y., Ashworth J.R., Clayton C.P., Parker R.P., Tarver E.D., Woolard N.F., High K.P. Prediction, progression, and outcomes of chronic kidney disease in older adults. J. Am. Soc. Nephrol. 2009, 20:1199-1209.
2. Baylis C., Corman B. The aging kidney: insights from experimental studies. J. Am. Soc. Nephrol. 1998, 9:699-709.
3. Bjorkoy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., Stenmark H., Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 2005, 171:603-614.
4. Bjorkoy G., Lamark T., Johansen T. p62/SQSTM1: a missing link between protein aggregates and the autophagy machinery. Autophagy 2006, 2:138-139.
5. Blagosklonny M.V. Calorie restriction decelerating mTOR-driven aging from cells to organisms (including humans). Cell Cycle 2010, 9:683-688.
6. Brunk U.T., Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur. J. Biochem. 2002, 269:1996-2002.
7. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 2000, 29:222-230.
8. Cao S.X., Dhahbi J.M., Mote P.L., Spindler S.R. Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10630-10635.
9. Cheng C.H., Chang H.R., Chiang C.W., Shu K.H., Chou M.C. Possible mechanism by which rapamycin increases cyclosporine nephrotoxicity. Transplant. Proc. 2008, 40:2373-2375.
10. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., Howitz K.T., Gorospe M., de Cabo R., Sinclair D.A. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004, 305:390-392.
11. Coresh J., Astor B.C., Greene T., Eknoyan G., Levey A.S. Prevalence of chronic kidney disease and decreased kidney function in the adult US population: Third National Health and Nutrition Examination Survey. Am. J. Kidney Dis. 2003, 41:1-12.
12. Cuervo A.M., Bergamini E., Brunk U.T., Droge W., Ffrench M., Terman A. Autophagy and aging: the importance of maintaining clean cells. Autophagy 2005, 1:131-140.
13. Cui J., Bai X.Y., Shi S., Cui S., Hong Q., Cai G., Chen X. Age-related changes in the function of autophagy in rat kidneys. Age (Dordr.) 2012, 34:329-339.
14. Cutler R.G. Human longevity and aging: possible role of reactive oxygen species. Ann. N. Y. Acad. Sci. 1991, 621:1-28.
15. Dhahbi J.M., Kim H.-J., Mote P.L., Beaver R.J., Spindler S.R. Temporal linkage between the phenotypic and genomic responses to caloric restriction. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:5524-5529.
16. Epstein M. Aging and the kidney. J. Am. Soc. Nephrol. 1996, 7:1106-1122.
17. Eskelinen E.L. Maturation of autophagic vacuoles in Mammalian cells. Autophagy 2005, 1:1-10.
18. Flores I., Blasco M.A. A p53-dependent response limits epidermal stem cell functionality and organismal size in mice with short telomeres. PLoS ONE 2009, 4:e4934.
19. Fraga C.G., Shigenaga M.K., Park J.W., Degan P., Ames B.N. Oxidative damage to DNA during aging: 8-hydroxy-2'-deoxyguanosine in rat organ DNA and urine. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:4533-4537.
20. Fulco M., Cen Y., Zhao P., Hoffman E.P., McBurney M.W., Sauve A.A., Sartorelli V. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 2008, 14:661-673.
21. Fulco M., Sartorelli V. Comparing and contrasting the roles of AMPK and SIRT1 in metabolic tissues. Cell Cycle 2008, 7:3669-3679.
22. Goto S. Health span extension by later-life caloric or dietary restriction: a view based on rodent studies. Biogerontology 2006, 7:135-138.
23. Hartleben B., Godel M., Meyer-Schwesinger C., Liu S., Ulrich T., Kobler S., Wiech T., Grahammer F., Arnold S.J., Lindenmeyer M.T., Cohen C.D., Pavenstadt H., Kerjaschki D., Mizushima N., Shaw A.S., Walz G., Huber T.B. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J. Clin. Invest. 2010, 120:1084-1096.
24. He C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 2009, 43:67-93.
25. Kadowaki M., Karim M.R. Cytosolic LC3 ratio as a quantitative index of macroautophagy. Methods Enzymol. 2009, 452:199-213.
26. Kawashima M., Kawakita T., Okada N., Ogawa Y., Murat D., Nakamura S., Nakashima H., Shimmura S., Shinmura K., Tsubota K. Calorie restriction: a new therapeutic intervention for age-related dry eye disease in rats. Biochem. Biophys. Res. Commun. 2010, 397:724-728.
27. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
28. Kitada M., Takeda A., Nagai T., Ito H., Kanasaki K., Koya D. Dietary restriction ameliorates diabetic nephropathy through anti-inflammatory effects and regulation of the autophagy via restoration of Sirt1 in diabetic Wistar fatty (fa/fa) rats: a model of type 2 diabetes. Exp. Diabetes Res. 2011, 2011:908185.
29. Komatsu M., Waguri S., Koike M., Sou Y.S., Ueno T., Hara T., Mizushima N., Iwata J., Ezaki J., Murata S., Hamazaki J., Nishito Y., Iemura S., Natsume T., Yanagawa T., Uwayama J., Warabi E., Yoshida H., Ishii T., Kobayashi A., Yamamoto M., Yue Z., Uchiyama Y., Kominami E., Tanaka K. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007, 131:1149-1163.
30. Krishnamurthty J., Torrice C., Ramsey M.R., Kovalev G.I., Al-Regaiey K., Su L.S., Sharpless N.E. Ink4a/Arf expression is a biomarker of aging. J. Clin. Invest. 2004, 114:1299-1307.
31. Kume S., Uzu T., Horiike K., Chin-Kanasaki M., Isshiki K., Araki S., Sugimoto T., Haneda M., Kashiwagi A., Koya D. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 2010, 120:1043-1055.
32. Levine B., Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6:463-477.
33. Liu S., Hartleben B., Kretz O., Wiech T., Igarashi P., Mizushima N., Walz G., Huber T.B. Autophagy plays a critical role in kidney tubule maintenance, aging and ischemia-reperfusion injury. Autophagy 2012, 8:826-837.
34. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2007, 8:741-752.
35. Martin-Montalvo A., de Cabo R. Mitochondrial metabolic reprogramming induced by calorie restriction. Antioxid. Redox Signal. 2013, 19(3):310-320.
36. Masoro E.J. Caloric restriction and aging: an update. Exp. Gerontol. 2000, 35:299-305.
37. Masoro E.J. Overview of caloric restriction and ageing. Mech. Ageing Dev. 2005, 126:913-922.
38. 2(-)) on physiological aging in C57BL/6J mice. J. Radiat. Res. 2009, 50:73-83.
39. Mizushima N., Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007, 3:542-545.
40. Pallet N., Bouvier N., Legendre C., Gilleron J., Codogno P., Beaune P., Thervet E., Anglicheau D. Autophagy protects renal tubular cells against cyclosporine toxicity. Autophagy 2008, 4:783-791.
41. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Overvatn A., Bjorkoy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
42. Rajawat Y.S., Hilioti Z., Bossis I. Aging: central role for autophagy and the lysosomal degradative system. Ageing Res. Rev. 2009, 8:199-213.
43. Rippe C., Lesniewski L., Connell M., LaRocca T., Donato A., Seals D. Short-term calorie restriction reverses vascular endothelial dysfunction in old mice by increasing nitric oxide and reducing oxidative stress. Aging Cell 2010, 9:304-312.
44. Sato S., Yanagihara T., Ghazizadeh M., Ishizaki M., Adachi A., Sasaki Y., Igarashi T., Fukunaga Y. Correlation of autophagy type in podocytes with histopathological diagnosis of IgA nephropathy. Pathobiology 2009, 76:221-226.
45. Seibenhener M.L., Babu J.R., Geetha T., Wong H.C., Krishna N.R., Wooten M.W. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 2004, 24:8055-8068.
46. Shigenaga M.K., Gimeno C.J., Ames B.N. Urinary 8-hydroxy-2'-deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:9697-9701.
47. Suzuki C., Isaka Y., Takabatake Y., Tanaka H., Koike M., Shibata M., Uchiyama Y., Takahara S., Imai E. Participation of autophagy in renal ischemia/reperfusion injury. Biochem. Biophys. Res. Commun. 2008, 368:100-106.
48. Takabatake Y., Isaka Y., Kimura T. The protective role of autophagy against aging and acute ischemic injury in kidney proximal tubular cells. Autophagy 2011, 7:1085-1087.
49. Takahashi A., Kimura T., Takabatake Y., Namba T., Kaimori J., Kitamura H., Matsui I., Niimura F., Matsusaka T., Fujita N., Yoshimori T., Isaka Y., Rakugi H. Autophagy guards against cisplatin-induced acute kidney injury. Am. J. Pathol. 2012, 180:517-525.
50. Terman A., Dalen H., Eaton J.W., Neuzil J., Brunk U.T. Mitochondrial recycling and aging of cardiac myocytes: the role of autophagocytosis. Exp. Gerontol. 2003, 38:863-876.
51. Terman A., Kurz T., Navratil M., Arriaga E.A., Brunk U.T. Mitochondrial turnover and aging of long-lived postmitotic cells: the mitochondrial-lysosomal axis theory of aging. Antioxid. Redox Signal. 2010, 12:503-535.
52. Tong Y., Yamaguchi H., Giaime E., Boyle S., Kopan R., Kelleher R.J., Shen J. Loss of leucine-rich repeat kinase 2 causes impairment of protein degradation pathways, accumulation of alpha-synuclein, and apoptotic cell death in aged mice. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:9879-9884.
53. Weindruch R., Sohal R.S. Seminars in medicine of the Beth Israel Deaconess Medical Center. Caloric intake and aging. N. Engl. J. Med. 1997, 337:986-994.
54. Wohlgemuth S.E., Julian D., Akin D.E., Fried J., Toscano K., Leeuwenburgh C., Dunn W.A. Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation Res. 2007, 10:281-292.
55. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
56. Yang C., Kaushal V., Shah S.V., Kaushal G.P. Autophagy is associated with apoptosis in cisplatin injury to renal tubular epithelial cells. Am J. Physiol. Renal Physiol. 2008, 294:F777-F787.