Long-Term Calorie Restriction Enhances Cellular Quality-Control Processes in Human Skeletal Muscle

Cell Reports

Volumn 14, Issue 3, 2016, Pages 422-428

  Yang, Ling ^a   Licastro, Danilo ^b   Cava, Edda ^c,d   Veronese, Nicola ^c,e   Spelta, Francesco ^c,f   Rizza, Wanda ^c,g   Bertozzi, Beatrice ^c   Villareal, Dennis T ^c,h   Hotamisligil, Gökhan S ^a   Holloszy, John O ^c   Fontana, Luigi ^c,i,j  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b Cluster in Biomedicine (CBM) scrl Genomics   (Italy)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e UNIVERSITY OF PADOVA   (Italy)

^f UNIVERSITY OF VERONA   (Italy)

^g UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^h MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF BRESCIA   (Italy)

^j CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

more..

Author keywords

Aldosterone; Autophagy; Calorie restriction; Cortisol; HSP70

Indexed keywords

ALDOSTERONE; BECLIN 1; CELL PROTEIN; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 70; HYDROCORTISONE; LIGHT CHAIN 3; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 1; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; LIGHT CHAIN 3, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MOLECULAR CHAPERONE GRP78; TRANSCRIPTION FACTOR;

ADULT; ALDOSTERONE BLOOD LEVEL; ARTICLE; ATHLETE; AUTOPHAGY; BODY HEIGHT; BODY MASS; BODY WEIGHT; CALORIC RESTRICTION; CONTROLLED STUDY; FEMALE; FOOD INTAKE; HUMAN; HUMAN EXPERIMENT; HYDROCORTISONE BLOOD LEVEL; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN QUALITY; SKELETAL MUSCLE; BLOOD; CLUSTER ANALYSIS; EXERCISE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; TIME FACTOR;

ADULT; APOPTOSIS REGULATORY PROTEINS; BECLIN-1; BODY MASS INDEX; CALORIC RESTRICTION; CLUSTER ANALYSIS; EXERCISE; FEMALE; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROCORTISONE; MALE; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MIDDLE AGED; MUSCLE, SKELETAL; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84953227268     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.12.042     Document Type: Article

References (40)

1. Anderson R.M., Shanmuganayagam D., Weindruch R. Caloric restriction and aging: studies in mice and monkeys. Toxicol. Pathol. 2009, 37:47-51.
2. Arumugam T.V., Phillips T.M., Cheng A., Morrell C.H., Mattson M.P., Wan R. Age and energy intake interact to modify cell stress pathways and stroke outcome. Ann. Neurol. 2010, 67:41-52.
3. Ben-Zvi A., Miller E.A., Morimoto R.I. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Natl. Acad. Sci. USA 2009, 106:14914-14919.
4. Braun T.P., Marks D.L. The regulation of muscle mass by endogenous glucocorticoids. Front. Physiol. 2015, 6:12.
5. Busillo J.M., Cidlowski J.A. The five Rs of glucocorticoid action during inflammation: ready, reinforce, repress, resolve, and restore. Trends Endocrinol. Metab. 2013, 24:109-119.
6. Csiszar A., Sosnowska D., Tucsek Z., Gautam T., Toth P., Losonczy G., Colman R.J., Weindruch R., Anderson R.M., Sonntag W.E., Ungvari Z. Circulating factors induced by caloric restriction in the nonhuman primate Macaca mulatta activate angiogenic processes in endothelial cells. J. Gerontol. A Biol. Sci. Med. Sci. 2013, 68:235-249.
7. Cuervo A.M. Calorie restriction and aging: the ultimate "cleansing diet.". J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:547-549.
8. de Cabo R., Fürer-Galbán S., Anson R.M., Gilman C., Gorospe M., Lane M.A. An in vitro model of caloric restriction. Exp. Gerontol. 2003, 38:631-639.
9. De Taeye B.M., Novitskaya T., McGuinness O.P., Gleaves L., Medda M., Covington J.W., Vaughan D.E. Macrophage TNF-alpha contributes to insulin resistance and hepatic steatosis in diet-induced obesity. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E713-E725.
10. Fontana L., Partridge L., Longo V.D. Extending healthy life span-from yeast to humans. Science 2010, 328:321-326.
11. Fontana L., Villareal D.T., Das S.K., Smith S.R., Meydani S.N., Pittas A.G., Klein S., Bhapkar M., Rochon J., Ravussin E., Holloszy J.O., CALERIE Study Group. Effects of 2-year calorie restriction on circulating levels of IGF-1, IGF-binding proteins and cortisol in nonobese men and women: a randomized clinical trial. Aging Cell 2015, Published online October 6, 2015. 10.1111/acel.12400.
12. Heydari A.R., You S., Takahashi R., Gutsmann A., Sarge K.D., Richardson A. Effect of caloric restriction on the expression of heat shock protein 70 and the activation of heat shock transcription factor 1. Dev. Genet. 1996, 18:114-124.
13. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
14. Hotamisligil G.S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
15. Hsu A.L., Murphy C.T., Kenyon C. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003, 300:1142-1145.
16. Kayani A.C., Close G.L., Broome C.S., Jackson M.J., McArdle A. Enhanced recovery from contraction-induced damage in skeletal muscles of old mice following treatment with the heat shock protein inducer 17-(allylamino)-17-demethoxygeldanamycin. Rejuvenation Res. 2008, 11:1021-1030.
17. Lee S., Notterpek L. Dietary restriction supports peripheral nerve health by enhancing endogenous protein quality control mechanisms. Exp. Gerontol. 2013, 48:1085-1090.
18. Levay E.A., Tammer A.H., Penman J., Kent S., Paolini A.G. Calorie restriction at increasing levels leads to augmented concentrations of corticosterone and decreasing concentrations of testosterone in rats. Nutr. Res. 2010, 30:366-373.
19. Madeo F., Zimmermann A., Maiuri M.C., Kroemer G. Essential role for autophagy in life span extension. J. Clin. Invest. 2015, 125:85-93.
20. Mattson M.P. Dietary factors, hormesis and health. Ageing Res. Rev. 2008, 7:43-48.
21. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 2005, 62:670-684.
22. Mercken E.M., Carboneau B.A., Krzysik-Walker S.M., de Cabo R. Of mice and men: the benefits of caloric restriction, exercise, and mimetics. Ageing Res. Rev. 2012, 11:390-398.
23. Mercken E.M., Crosby S.D., Lamming D.W., JeBailey L., Krzysik-Walker S., Villareal D.T., Capri M., Franceschi C., Zhang Y., Becker K., et al. Calorie restriction in humans inhibits the PI3K/AKT pathway and induces a younger transcription profile. Aging Cell 2013, 12:645-651.
24. Morimoto R.I., Cuervo A.M. Proteostasis and the aging proteome in health and disease. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69(Suppl 1):S33-S38.
25. Munck A., Guyre P.M., Holbrook N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 1984, 5:25-44.
26. Omodei D., Licastro D., Salvatore F., Crosby S.D., Fontana L. Serum from humans on long-term calorie restriction enhances stress resistance in cell culture. Aging (Albany, N.Y.) 2013, 5:599-606.
27. Pashko L.L., Schwartz A.G. Inhibition of 7,12-dimethylbenz[a]anthracene-induced lung tumorigenesis in A/J mice by food restriction is reversed by adrenalectomy. Carcinogenesis 1996, 17:209-212.
28. Ravussin E., Redman L.M., Rochon J., Das S.K., Fontana L., Kraus W.E., Romashkan S., Williamson D.A., Meydani S.N., Villareal D.T., et al., CALERIE Study Group. A 2-year randomized controlled trial of human caloric restriction: feasibility and effects on predictors of health span and longevity. J. Gerontol. A Biol. Sci. Med. Sci. 2015, 70:1097-1104.
29. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
30. Selsby J.T., Judge A.R., Yimlamai T., Leeuwenburgh C., Dodd S.L. Life long calorie restriction increases heat shock proteins and proteasome activity in soleus muscles of Fisher 344 rats. Exp. Gerontol. 2005, 40:37-42.
31. Stewart J.W., Koehler K., Jackson W., Hawley J., Wang W., Au A., Myers R., Birt D.F. Prevention of mouse skin tumor promotion by dietary energy restriction requires an intact adrenal gland and glucocorticoid supplementation restores inhibition. Carcinogenesis 2005, 26:1077-1084.
32. Stricher F., Macri C., Ruff M., Muller S. HSPA8/HSC70 chaperone protein: structure, function, and chemical targeting. Autophagy 2013, 9:1937-1954.
33. Uysal K.T., Wiesbrock S.M., Marino M.W., Hotamisligil G.S. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 1997, 389:610-614.
34. Wang L., Fan J., Lin Y.S., Guo Y.S., Gao B., Shi Q.Y., Wei B.Y., Chen L., Yang L., Liu J., Luo Z.J. Glucocorticoids induce autophagy in rat bone marrow mesenchymal stem cells. Mol. Med. Rep. 2015, 11:2711-2716.
35. Wu D., Ren Z., Pae M., Guo W., Cui X., Merrill A.H., Meydani S.N. Aging up-regulates expression of inflammatory mediators in mouse adipose tissue. J. Immunol. 2007, 179:4829-4839.
36. Yaktine A.L., Vaughn R., Blackwood D., Duysen E., Birt D.F. Dietary energy restriction in the SENCAR mouse: elevation of glucocorticoid hormone levels but no change in distribution of glucocorticoid receptor in epidermal cells. Mol. Carcinog. 1998, 21:62-69.
37. Yang L., Li P., Fu S., Calay E.S., Hotamisligil G.S. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010, 11:467-478.
38. Yang L., Calay E.S., Fan J., Arduini A., Kunz R.C., Gygi S.P., Yalcin A., Fu S., Hotamisligil G.S. Metabolism. S-nitrosylation links obesity-associated inflammation to endoplasmic reticulum dysfunction. Science 2015, 349:500-506.
39. Yokoyama K., Fukumoto K., Murakami T., Harada S., Hosono R., Wadhwa R., Mitsui Y., Ohkuma S. Extended longevity of Caenorhabditis elegans by knocking in extra copies of hsp70F, a homolog of mot-2 (mortalin)/mthsp70/Grp75. FEBS Lett. 2002, 516:53-57.
40. Yu Z.F., Mattson M.P. Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J. Neurosci. Res. 1999, 57:830-839.