Metabolic effects of fasting on human and mouse blood in vivo

Autophagy

Volumn 13, Issue 3, 2017, Pages 567-578

  Pietrocola, Federico ^a,b,c,d   Demont, Yohann ^a,b,c   Castoldi, Francesca ^a,b,c,d,f   Enot, David ^a,d   Durand, Sylvère ^a,d   Semeraro, Michaela ^a,e   Baracco, Elisa Elena ^a,b,c,d   Pol, Jonathan ^a,b,c,d   Bravo San Pedro, Jose Manuel ^a,b,c,d   Bordenave, Chloé ^a,d   Levesque, Sarah ^a,b,c,d   Humeau, Juliette ^a,b,c,d   Chery, Alexis ^a,d   Métivier, Didier ^a,b,c   Madeo, Frank ^g,h   Maiuri, M Chiara ^a,b,c,d   Kroemer, Guido ^a,b,c,d,i,j  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

^e ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^f Sotio   (Czech Republic)

^g UNIVERSITY OF GRAZ   (Austria)

^h BIOTECHMED GRAZ   (Austria)

ⁱ HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^j KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

more..

Author keywords

autophagy; caloric restriction; IGF1; leukocytes; longevity; metabolome; p62; protein acetylation

Indexed keywords

BIOCHEMICAL MARKER; LEUPEPTIN; LYSINE; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 BETA; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; BLOOD CELL; BLOOD SAMPLING; CALORIC RESTRICTION; CELL ACTIVATION; CELL NUCLEUS; CELL SUBPOPULATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOFLUOROMETRY; CYTOPLASM; DEACETYLATION; DIET RESTRICTION; FEMALE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VIVO STUDY; LEUKOCYTE; LEUKOCYTE CULTURE; LIGHT CHAIN; MALE; METABOLOME; METABOLOMICS; MOUSE; NEUTROPHIL; NONHUMAN; NORMAL HUMAN; PROTEIN ACETYLATION; STARVATION; WEIGHT REDUCTION; ACETYLATION; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CLINICAL TRIAL; METABOLISM; MIDDLE AGED; YOUNG ADULT;

ACETYLATION; ADULT; ANIMALS; AUTOPHAGY; CELLS, CULTURED; FASTING; FEMALE; HUMANS; LYSINE; MALE; METABOLOME; METABOLOMICS; MICE, INBRED C57BL; MIDDLE AGED; NEUTROPHILS; STARVATION; YOUNG ADULT;

EID: 85011662390     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1271513     Document Type: Article

References (56)

1. Mizushima N, Klionsky DJ. Protein turnover via autophagy:implications for metabolism. Annu Rev Nutr 2007; 27:19-40; PMID:17311494; http://dx.doi.org/10.1146/annurev.nutr.27.061406.093749
2. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi.org/10.1146/annurev-genet-102808-114910
3. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; http://dx.doi.org/10.1038/nature09782
4. Shen HM, Mizushima N. At the end of the autophagic road:an emerging understanding of lysosomal functions in autophagy. Trends Biochem Sci 2014; 39:61-71; PMID:24369758; http://dx.doi.org/10.1016/j.tibs.2013.12.001
5. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, Codogno P, Debnath J, Gewirtz DA, Karantza V, et al. Autophagy in malignant transformation and cancer progression. EMBO J 2015; 34:856-80; PMID:25712477; http://dx.doi.org/10.15252/embj.201490784
6. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 2003; 301:1387-91.
7. Tavernarakis N, Pasparaki A, Tasdemir E, Maiuri MC, Kroemer G. The effects of p53 on whole organism longevity are mediated by autophagy. Autophagy 2008; 4:870-3; PMID:18728385; http://dx.doi.org/10.4161/auto.6730
8. Eisenberg T, Knauer H, Schauer A, Buttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 2009; 11:1305-14; PMID:19801973; http://dx.doi.org/10.1038/ncb1975
9. Morselli E, Maiuri MC, Markaki M, Megalou E, Pasparaki A, Palikaras K, Criollo A, Galluzzi L, Malik SA, Vitale I. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 2010; 1:e10; PMID:21364612; http://dx.doi.org/10.1038/cddis.2009.8
10. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, Foley A, Partridge L. Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab 2010; 11:35-46; PMID:20074526; http://dx.doi.org/10.1016/j.cmet.2009.11.010
11. Rubinsztein DC, Marino G, Kroemer G. Autophagy and aging. Cell 2011; 146:682-95; PMID:21884931; http://dx.doi.org/10.1016/j.cell.2011.07.030
12. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013; 153:1194-217; PMID:23746838; http://dx.doi.org/10.1016/j.cell.2013.05.039
13. Madeo F, Zimmermann A, Maiuri MC, Kroemer G. Essential role for autophagy in life span extension. J Clin Invest 2015; 125:85-93; PMID:25654554; http://dx.doi.org/10.1172/JCI73946
14. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
15. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
16. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 2016; 12:1-222; PMID:26799652; http://dx.doi.org/10.1080/15548627.2015.1100356
17. Rubinsztein DC, Cuervo AM, Ravikumar B, Sarkar S, Korolchuk V, Kaushik S, Klionsky DJ. In search of an "autophagomometer". Autophagy 2009; 5:585-9; PMID:19411822; http://dx.doi.org/10.4161/auto.5.5.8823
18. Ju JS, Varadhachary AS, Miller SE, Weihl CC. Quantitation of "autophagic flux" in mature skeletal muscle. Autophagy 2010; 6:929-35; PMID:20657169; http://dx.doi.org/10.4161/auto.6.7.12785
19. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 2004; 15:1101-11; PMID:14699058; http://dx.doi.org/10.1091/mbc.E03-09-0704
20. Imai S, Guarente L. NAD+ and sirtuins in aging and disease. Trends Cell Biol 2014; 24:464-71; PMID:24786309; http://dx.doi.org/10.1016/j.tcb.2014.04.002
21. Marino G, Pietrocola F, Eisenberg T, Kong Y, Malik SA, Andryushkova A, Schroeder S, Pendl T, Harger A, Niso-Santano M, et al. Regulation of autophagy by cytosolic acetyl-coenzyme A. Mol Cell 2014; 53:710-25; PMID:24560926; http://dx.doi.org/10.1016/j.molcel.2014.01.016
22. Madeo F, Pietrocola F, Eisenberg T, Kroemer G. Caloric restriction mimetics:towards a molecular definition. Nat Rev Drug Discov 2014; 13:727-40; PMID:25212602; http://dx.doi.org/10.1038/nrd4391
23. Pietrocola F, Lachkar S, Enot DP, Niso-Santano M, Bravo-San Pedro JM, Sica V, Izzo V, Maiuri MC, Madeo F, Mariño G. Spermidine induces autophagy by inhibiting the acetyltransferase EP300. Cell Death Differ 2015; 22:509-16; PMID:25526088; http://dx.doi.org/10.1038/cdd.2014.215
24. Kim H, Golub GH, Park H. Missing value estimation for DNA microarray gene expression data:local least squares imputation. Bioinformatics 2005; 21:187-98; PMID:15333461; http://dx.doi.org/10.1093/bioinformatics/bth499
25. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 2015; 43:e47; PMID:25605792; http://dx.doi.org/10.1093/nar/gkv007
26. Pietrocola F, Pol J, Vacchelli E, Baracco EE, Levesque S, Castoldi F, Maiuri MC, Madeo F, Kroemer G. Autophagy induction for the treatment of cancer. Autophagy 2016:12:1962-1964.
27. Hariharan N, Maejima Y, Nakae J, Paik J, Depinho RA, Sadoshima J. Deacetylation of FoxO by Sirt1 Plays an Essential Role in Mediating Starvation-Induced Autophagy in Cardiac Myocytes. Circ Res 2010; 107:1470-82; PMID:20947830; http://dx.doi.org/10.1161/CIRCRESAHA.110.227371
28. Longo VD. Linking sirtuins, IGF-I signaling, and starvation. Exp Gerontol 2009; 44:70; PMID:18638538; http://dx.doi.org/10.1016/j.exger.2008.06.005
29. Fendl B, Weiss R, Fischer MB, Spittler A, Weber V. Characterization of extracellular vesicles in whole blood:Influence of pre-analytical parameters and visualization of vesicle-cell interactions using imaging flow cytometry. Biochem Biophys Res Commun 2016; 478:168-73; PMID:27444383; http://dx.doi.org/10.1016/j.bbrc.2016.07.073
30. Samsel L, Dagur PK, Raghavachari N, Seamon C, Kato GJ, McCoy JP, Jr. Imaging flow cytometry for morphologic and phenotypic characterization of rare circulating endothelial cells. Cytometry B Clin Cytom 2013; 84:379-89; PMID:23554273; http://dx.doi.org/10.1002/cyto.b.21088
31. Clark RT. Imaging flow cytometry enhances particle detection sensitivity for extracellular vesicle analysis; Nature Methods 2015; 12; PMID:27444383; http://dx.doi.org/10.1038/nmeth.3321
32. Eisenberg T, Schroeder S, Andryushkova A, Pendl T, Kuttner V, Bhukel A, Mariño G, Pietrocola F, Harger A, Zimmermann A, et al. Nucleocytosolic depletion of the energy metabolite acetyl-coenzyme a stimulates autophagy and prolongs lifespan. Cell Metab 2014; 19:431-44; PMID:24606900; http://dx.doi.org/10.1016/j.cmet.2014.02.010
33. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3:542-5; PMID:17611390; http://dx.doi.org/10.4161/auto.4600
34. Bjorkoy G, Lamark T, Pankiv S, Overvatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452:181-97; PMID:19200883; http://dx.doi.org/10.1016/S0076-6879(08)03612-4
35. Komatsu M, Ichimura Y. Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 2010; 584:1374-8; PMID:20153326; http://dx.doi.org/10.1016/j.febslet.2010.02.017
36. Sahani MH, Itakura E, Mizushima N. Expression of the autophagy substrate SQSTM1/p62 is restored during prolonged starvation depending on transcriptional upregulation and autophagy-derived amino acids. Autophagy 2014; 10:431-41; PMID:24394643; http://dx.doi.org/10.4161/auto.27344
37. Mofarrahi M, Guo Y, Haspel JA, Choi AM, Davis EC, Gouspillou G, Hepple RT, Godin R, Burelle Y, Hussain SN. Autophagic flux and oxidative capacity of skeletal muscles during acute starvation. Autophagy 2013; 9:1604-20; PMID:23955121; http://dx.doi.org/10.4161/auto.25955
38. Esteban-Martinez L, Boya P. Autophagic flux determination in vivo and ex vivo. Methods 2015; 75:79-86; PMID:25644445; http://dx.doi.org/10.1016/j.ymeth.2015.01.008
39. Phadwal K, Alegre-Abarrategui J, Watson AS, Pike L, Anbalagan S, Hammond EM, Wade-Martins R, McMichael A, Klenerman P, Simon AK. A novel method for autophagy detection in primary cells:impaired levels of macroautophagy in immunosenescent T cells. Autophagy 2012; 8:677-89; PMID:22302009; http://dx.doi.org/10.4161/auto.18935
40. Finn PF, Dice JF. Proteolytic and lipolytic responses to starvation. Nutrition 2006; 22:830-44; PMID:16815497; http://dx.doi.org/10.1016/j.nut.2006.04.008
41. Cahill, GF, Jr. Fuel metabolism in starvation. Annu Rev Nutr 2006; 26:1-22; PMID:16848698; http://dx.doi.org/10.1146/annurev.nutr.26.061505.111258
42. Bouwens M, Afman LA, Muller M. Fasting induces changes in peripheral blood mononuclear cell gene expression profiles related to increases in fatty acid beta-oxidation:functional role of peroxisome proliferator activated receptor alpha in human peripheral blood mononuclear cells. Am J Clin Nutr 2007; 86:1515-23; PMID:17991667
43. Hildebrandt W, Kinscherf R, Hauer K, Holm E, Droge W. Plasma cystine concentration and redox state in aging and physical exercise. Mech Ageing Dev 2002; 123:1269-81; PMID:12020948; http://dx.doi.org/10.1016/S0047-6374(02)00013-1
44. Hine C, Harputlugil E, Zhang Y, Ruckenstuhl C, Lee BC, Brace L, Longchamp A, Treviño-Villarreal JH, Mejia P, Ozaki CK, et al. Endogenous hydrogen sulfide production is essential for dietary restriction benefits. Cell 2015; 160:132-44; PMID:25542313; http://dx.doi.org/10.1016/j.cell.2014.11.048
45. Green DR, Galluzzi L, Kroemer G. Cell biology. Metabolic control of cell death. Science 2014; 345:1250256.
46. Galluzzi L, Pietrocola F, Levine B, Kroemer G. Metabolic control of autophagy. Cell 2014; 159:1263-76; PMID:25480292; http://dx.doi.org/10.1016/j.cell.2014.11.006
47. Lee C, Safdie FM, Raffaghello L, Wei M, Madia F, Parrella E, Hwang D, Cohen P, Bianchi G, Longo VD. Reduced levels of IGF-I mediate differential protection of normal and cancer cells in response to fasting and improve chemotherapeutic index. Cancer Res 2010; 70:1564-72; PMID:20145127; http://dx.doi.org/10.1158/0008-5472.CAN-09-3228
48. Longo VD, Fontana L. Calorie restriction and cancer prevention:metabolic and molecular mechanisms. Trends Pharmacol Sci 2010; 31:89-98; PMID:20097433; http://dx.doi.org/10.1016/j.tips.2009.11.004
49. Lee JV, Carrer A, Shah S, Snyder NW, Wei S, Venneti S, Worth AJ, Yuan ZF, Lim HW, Liu S, et al. Akt-dependent metabolic reprogramming regulates tumor cell histone acetylation. Cell Metab 2014; 20:306-19; PMID:24998913; http://dx.doi.org/10.1016/j.cmet.2014.06.004
50. Comerford SA, Huang Z, Du X, Wang Y, Cai L, Witkiewicz AK, Walters H, Tantawy MN, Fu A, Manning HC, et al. Acetate dependence of tumors. Cell 2014; 159:1591-602; PMID:25525877; http://dx.doi.org/10.1016/j.cell.2014.11.020
51. Mashimo T, Pichumani K, Vemireddy V, Hatanpaa KJ, Singh DK, Sirasanagandla S, Nannepaga S, Piccirillo SG, Kovacs Z, Foong C, et al. Acetate is a bioenergetic substrate for human glioblastoma and brain metastases. Cell 2014; 159:1603-14; PMID:25525878; http://dx.doi.org/10.1016/j.cell.2014.11.025
52. Wang Z, Cao L, Kang R, Yang M, Liu L, Zhao Y, Yu Y, Xie M, Yin X, Livesey KM, et al. Autophagy regulates myeloid cell differentiation by p62/SQSTM1-mediated degradation of PML-RARalpha oncoprotein. Autophagy 2011; 7:401-11; PMID:21187718; http://dx.doi.org/10.4161/auto.7.4.14397
53. Orfanelli T, Doulaveris G, Holcomb K, Jeong JM, Sisti G, Kanninen TT, Caputo TA, Gupta D, Witkin SS. Inhibition of autophagy in peripheral blood mononuclear cells by vaginal fluid from women with a malignant adnexal mass. Int J Cancer 2015; 137:2879-84; PMID:26132572; http://dx.doi.org/10.1002/ijc.29665
54. Leveque-El Mouttie L, Vu T, Lineburg KE, Kuns RD, Bagger FO, Teal BE, Lor M, Boyle GM, Bruedigam C, Mintern JD, et al. Autophagy is required for stem cell mobilization by G-CSF. Blood 2015; 125:2933-6; PMID:25788702; http://dx.doi.org/10.1182/blood-2014-03-562660
55. Remijsen Q, Vanden Berghe T, Wirawan E, Asselbergh B, Parthoens E, De Rycke R, Noppen S, Delforge M, Willems J, Vandenabeele P. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res 2011; 21:290-304; PMID:21060338; http://dx.doi.org/10.1038/cr.2010.150
56. Francois A, Julian A, Ragot S, Dugast E, Blanchard L, Brishoual S, Terro F, Chassaing D, Page G, Paccalin M. Inflammatory Stress on Autophagy in Peripheral Blood Mononuclear Cells from Patients with Alzheimer's Disease during 24 Months of Follow-Up. PLoS One 2015; 10:e0138326; PMID:26393801; http://dx.doi.org/10.1371/journal.pone.0138326